Phylogeny of Penicillium and the segregation of Trichocomaceae into three families.
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Abstract
Taxonomic novelties
New sections, all in Penicillium: sect. Sclerotiora Houbraken & Samson, sect. Charlesia Houbraken & Samson, sect. Thysanophora Houbraken & Samson,sect. Ochrosalmonea Houbraken & Samson, sect. Cinnamopurpurea Houbraken & Samson, Fracta Houbraken & Samson, sect. Stolkia Houbraken & Samson, sect. Gracilenta Houbraken & Samson, sect. Citrina Houbraken & Samson, sect. Turbata Houbraken & Samson, sect. Paradoxa Houbraken & Samson, sect. Canescentia Houbraken & Samson. New combinations:Penicillium asymmetricum (Subramanian & Sudha) Houbraken & Samson, P. bovifimosum (Tuthill & Frisvad) Houbraken & Samson, P. glaucoalbidum (Desmazières) Houbraken & Samson, P. laeve (K. Ando & Manoch) Houbraken & Samson, P. longisporum (Kendrick) Houbraken & Samson, P. malachiteum (Yaguchi & Udagawa) Houbraken & Samson, P. ovatum (K. Ando & Nawawi) Houbraken & Samson, P. parviverrucosum (K. Ando & Pitt) Houbraken & Samson, P. saturniforme (Wang & Zhuang) Houbraken & Samson, P. taiwanense (Matsushima) Houbraken & Samson. New names:Penicillium coniferophilum Houbraken & Samson, P. hennebertii Houbraken & Samson, P. melanostipe Houbraken & Samson, P. porphyreum Houbraken & Samson.Free full text
Phylogeny of Penicillium and the segregation of Trichocomaceae into three families
Associated Data
Abstract
Species of Trichocomaceae occur commonly and are important to both industry and medicine. They are associated with food spoilage and mycotoxin production and can occur in the indoor environment, causing health hazards by the formation of β-glucans, mycotoxins and surface proteins. Some species are opportunistic pathogens, while others are exploited in biotechnology for the production of enzymes, antibiotics and other products. Penicillium belongs phylogenetically to Trichocomaceae and more than 250 species are currently accepted in this genus. In this study, we investigated the relationship of Penicillium to other genera of Trichocomaceae and studied in detail the phylogeny of the genus itself. In order to study these relationships, partial RPB1, RPB2 (RNA polymerase II genes), Tsr1 (putative ribosome biogenesis protein) and Cct8 (putative chaperonin complex component TCP-1) gene sequences were obtained. The Trichocomaceae are divided in three separate families: Aspergillaceae, Thermoascaceae and Trichocomaceae. The Aspergillaceae are characterised by the formation flask-shaped or cylindrical phialides, asci produced inside cleistothecia or surrounded by Hülle cells and mainly ascospores with a furrow or slit, while the Trichocomaceae are defined by the formation of lanceolate phialides, asci borne within a tuft or layer of loose hyphae and ascospores lacking a slit. Thermoascus and Paecilomyces, both members of Thermoascaceae, also form ascospores lacking a furrow or slit, but are differentiated from Trichocomaceae by the production of asci from croziers and their thermotolerant or thermophilic nature. Phylogenetic analysis shows that Penicillium is polyphyletic. The genus is re-defined and a monophyletic genus for both anamorphs and teleomorphs is created (Penicillium sensu stricto). The genera Thysanophora, Eupenicillium, Chromocleista, Hemicarpenteles and Torulomyces belong in Penicillium s. str. and new combinations for the species belonging to these genera are proposed. Analysis of Penicillium below genus rank revealed the presence of 25 clades. A new classification system including both anamorph and teleomorph species is proposed and these 25 clades are treated here as sections. An overview of species belonging to each section is presented.
Taxonomic novelties:
New sections, all in Penicillium: sect. Sclerotiora Houbraken & Samson, sect. Charlesia Houbraken & Samson, sect. Thysanophora Houbraken & Samson,sect. Ochrosalmonea Houbraken & Samson, sect. Cinnamopurpurea Houbraken & Samson, Fracta Houbraken & Samson, sect. Stolkia Houbraken & Samson, sect. Gracilenta Houbraken & Samson, sect. Citrina Houbraken & Samson, sect. Turbata Houbraken & Samson, sect. Paradoxa Houbraken & Samson, sect. Canescentia Houbraken & Samson.
New combinations: Penicillium asymmetricum (Subramanian & Sudha) Houbraken & Samson, P. bovifimosum (Tuthill & Frisvad) Houbraken & Samson, P. glaucoalbidum (Desmazières) Houbraken & Samson, P. laeve (K. Ando & Manoch) Houbraken & Samson, P. longisporum (Kendrick) Houbraken & Samson, P. malachiteum (Yaguchi & Udagawa) Houbraken & Samson, P. ovatum (K. Ando & Nawawi) Houbraken & Samson, P. parviverrucosum (K. Ando & Pitt) Houbraken & Samson, P. saturniforme (Wang & Zhuang) Houbraken & Samson, P. taiwanense (Matsushima) Houbraken & Samson.
New names: Penicillium coniferophilum Houbraken & Samson, P. hennebertii Houbraken & Samson, P. melanostipe Houbraken & Samson, P. porphyreum Houbraken & Samson.
INTRODUCTION
The Trichocomaceae comprise a relatively large family of fungi well-known for their impact, both positive and negative, on human activities. The most well-known species of this family belong to the genera Aspergillus, Penicillium and Paecilomyces. Species belonging to Trichocomaceae are predominantly saprobic and represent some of the most catabolically and anabolically diverse microorganisms known. Some species are capable of growing at extremely low water activities (i.e. xerotolerant and/or osmotolerant), low temperatures (psychrotolerant) and high temperatures (thermotolerant). Members of Trichocomaceae secrete secondary metabolites (extrolites) that are known as mycotoxins (e.g. aflatoxins, ochratoxins, patulin), while other extrolites are used as pharmaceuticals, including antibiotics such as penicillin and the cholesterol-lowering agent lovastatin. Furthermore, members of Trichocomaceae are also known for their production of organic acids and diverse enzymes that degrade a wide variety of complex biomolecules (Geiser et al. 2006, Pitt & Hocking 2009, Samson et al. 2010).
The taxon Trichocomaceae was introduced by Fischer (1897) and the classification of this family was studied extensively using phenotypic characters (Malloch & Cain 1972, Subramanian 1972, Malloch 1985a, b, von Arx1986). These studies include only teleomorph genera because Trichocomaceae is based on Trichocoma, a teleomorph genus, and thus not applicable for anamorph genera (Malloch 1985b). However, it is noted that anamorph genera with phialidic structures are linked to Trichocomaceae (Malloch & Cain 1972). Currently, only the phylogenetic relationships within certain genera of Trichocomaceae, e.g. Aspergillus, Penicillium and Paecilomyces, are elucidated (Peterson 2000a, b, Samson et al. 2004, Peterson 2008, Samson et al. 2009), but the relationships among the genera are still poorly studied.
Penicillium is an anamorph genus and belongs phylogenetically to Trichocomaceae (Berbee 1995, Peterson 2000a). The name Penicillium is derived from penicillus, which means “little brush” and was introduced by Link in 1809. Many new species were described in the 19th century, and Dierckx (1901) was the first researcher who introduced a subgeneric classification system for the genus.
He proposed the subgenera Aspergilloides, Biverticillium and Eupenicillium and Biourge (1923) followed Dierckx's classification system and expanded it with two sections, four series and six subsections. Thom (1930: 155–159) did not accept Dierckx's and Biourge's subgeneric classification system and introduced a new system with four divisions (subgenera), 12 sections and 18 subsections (series). His system was mainly based on colony characteristics and conidiophore branching and the monographs of Raper & Thom (1949) and Ramírez (1982) are in line with that of Thom (1930). Pitt (1980) did not follow Thom's concept and, based on conidiophore characters, phialide shapes and growth characteristics, divided Penicillium into four subgenera, 10 sections and 21 series. In addition, he treated Eupenicillium separately from Penicillium and subdivided the former genus into eight series. In 1985, Stolk & Samson proposed another taxonomic scheme for Penicillium anamorphs and this classification was primary based on phialide shape and conidiophore branching. They divided Penicillium in 10 sections and 18 series and this taxonomic scheme treated strict anamorphs, as well as anamorphs of sexual Penicillium species. More recently, Frisvad & Samson (2004) studied subgenus Penicillium and five sections and 17 series were recognised.
The first attempt to make a subgeneric classification of Eupenicillium was undertaken by Pitt (1980) and eight series were introduced. This classification was based on a combination of various characters, such as growth rates in standard conditions, colony morphology and microscopical characters of both teleomorphic and anamorphic states. In the monograph of Stolk & Samson (1983), four sections were introduced for the classification of Eupenicillium, and Pitt's concept of using series of species was abandoned.
To date, only a limited number of studies have investigated the phylogenetic relationship of Penicillium at genus level. Berbee (1995), based of 18S rDNA sequences, demonstrated that Penicillium is polyphyletic. The genus splits up in two clades: one clade includes Talaromyces species and members of the subgenus Biverticillium and the other clade includes Eupenicillium species and Penicillium species accommodated in the subgenera Penicillium, Furcatum and Aspergilloides (LoBuglio & Taylor 1993, LoBuglio et al. 1993, Berbee et al. 1995, Ogawa et al. 1997, Wang & Zhuang 2007). Peterson (2000a) studied the phylogeny of Eupenicillium and members of the subgenera Penicillium, Furcatum and Aspergilloides in more detail. He subsequently divided the studied species in six groups and showed that many subgeneric taxa in Penicillium are polyphyletic. Furthermore, his data indicated that the current classification systems based on conidiophore branching is not congruent with the phylogeny and a new subgeneric classification system is needed.
Pleomorphism in fungi was first demonstrated by Tulasne (1851). Together with his discovery, he was already aware of the problem raised by the nomenclature of composite species and he stated that the imperfect forms must someday be submerged in the Ascomycota. He thus established a first principle of pleomorphic nomenclature and suggested the precedence of the perfect state name over imperfect names (Hennebert 1971). In 1910, “dual nomenclature” was introduced and this was established in the International Code of Botanical Nomenclature (ICBN). The problem of naming fungi that exhibit pleomorphic life cycles was addressed in previous versions of article 59 of the ICBN and implied that more than one name for a single taxon can be used (Cline 2005). Recently, the proposal to revise article 59 was accepted at the 2011 IBC Nomenclature Section at Melbourne and the principle of “one fungus: one name” was established (Norvell et al. 2011).
In the present study, the phylogenetic relationships between Penicillium and other members of the family Trichocomaceae are studied using a combined analysis of four loci (RPB1, RPB2, Tsr1 and Cct8). In this study, the principle “one fungus- one name” is applied and priority is given to the oldest family, genus and section names using the single-name nomenclature (Hawksworth et al. 2011, Norvell 2011). Penicillium is delimited, various genera are placed in synonymy, and new combinations in Penicillium are made for the species belonging to the genera Thysanophora, Eupenicillium, Chromocleista, Hemicarpenteles and Torulomyces. Subsequently, the phylogeny of Penicillium is studied and a new sectional classification system is proposed. In addition, an overview of species in each section is presented.
MATERIAL AND METHODS
Strains
The first part of this study treats the phylogenetic relationships of the Penicillium species among Trichocomaceae. A selection of strains is made in order to study these relationships and in most cases the types of the genera were selected. The second part deals with the phylogeny of Penicillium. For this study, the type species of the various subgenera and sections in Penicillium and Eupenicillium were selected, and this selection is supplemented with other related species. An overview of strains used in the study of the phylogeny of Trichocomaceae and Penicillium presented in Table 1. In the third part of this study, a new sectional classification system for Penicillium is proposed and lists of species in each section are compiled. For the preparation of these lists, mostly type strains were selected of accepted Penicillium and Eupenicillium species. This selection is based on the overview of “accepted species and their synonyms in the Trichocomaceae” by Pitt et al. (2000) and supplemented with species described after 2000. An overview of these strains is shown in Table S1 (Supplementary Information- online only) and partly in Table 1 (species names indicated with two asterisks). All strains are maintained in the CBS-KNAW culture collection and additional strains were obtained from IBT (culture collection of Center for Microbial Biotechnology (CMB) at Department of Systems Biology, Technical University of Denmark), NRRL (ARS Culture Collection, U.S. Department of Agriculture, Peoria, Illinois, USA), ATCC (American Type Culture Collection, Manassas, VA, USA) and IMI (CABI Genetic Resources Collection, Surrey, UK).
Table 1
Strains used in phylogenetic analysis of Trichocomaceae and other families.
| CBS no. | Name | Other collections | Origin | GenBank accession or reference1 | |||
|---|---|---|---|---|---|---|---|
| RPB1 | RPB2 | Tsr1 | Cct8 | ||||
| CBS 267.72NT | Aphanoascus cinnabarinus* | ATCC 26215 | Soil, Japan | JN121625 | JN121477 | JN121783 | JN121903 |
| CBS 172.66T | Aspergillus aculeatus* | ATCC 16872 = IMI 211388 | Tropical soil | JN121590 | JN121448 | JN121755 | JN121895 |
| CBS 600.67T | Aspergillus amylovorus* | ATCC 18351 = IMI 129961 = MUCL 15648 | Wheat starch, Kharkiv, Ukraine | JN121705 | JN121538 | JN121844 | JN121931 |
| CBS 463.65NT | Aspergillus arenarius* | ATCC 16830 = IMI 055632 = IMI 055632ii | Soil, Mysore, Karnataka, India | JN121684 | JN121520 | JN121825 | JN121917 |
| CBS 653.74T | Aspergillus aureofulgens* | Natural truffle soil, Provence, France | JN121712 | JN121545 | JN121851 | JN121936 | |
| CBS 109.46NT | Aspergillus avenaceus* | ATCC 16861 = IMI 016140 = NRRL 517 | Seed of Pisum sativum (pea), England, UK | JN121565 | JN121424 | JN121731 | JN121878 |
| CBS 468.65NT | Aspergillus biplanus* | ATCC 16858 = IMI 235602 | Soil, Tilaran, Costa Rica | JN121685 | JN121520 | JN121826 | JN121917 |
| CBS 707.71T | Aspergillus bisporus* | ATCC 22527 = NRRL 3693 | Soil injected into mouse, Clarksburg, Maryland, USA | JN121715 | JN121548 | JN121854 | JN121939 |
| CBS 127.61NT | Aspergillus brunneouniseriatus* | ATCC 16916 = IMI 227677 | Soil under Dalbergia sissoo, India | JN121583 | JN121442 | JN121749 | JN121889 |
| CBS 121611 | Aspergillus calidoustus* | Patient (case 4), man with allogeneic HSCT, probably lung infection, man, Washington, USA | JN121579 | JN121438 | JN121745 | JN121887 | |
| CBS 566.65NT | Aspergillus candidus* | ATCC 1002 = IMI 091889 = NRRL 303 | Unknown source | JN121702 | JN121535 | JN121841 | JN121929 |
| CBS 196.64NT | Aspergillus cervinus* | ATCC 15508 = IMI 107684 | Soil, West Malaysia, Malaysia | JN121595 | JN121452 | JN121759 | JN121896 |
| CBS 473.65NT | Aspergillus clavatoflavus* | ATCC 16866 = IMI 124937 | Rain forest soil,Tulley, Queensland, Australia | JN121686 | JN121521 | JN121827 | JN121918 |
| Aspergillus clavatus1* | NRRL 1 (= ATCC 1007 = CBS 513.65 = IMI 15949) | Unknown source | Fedorova et al. (2008) | ||||
| CBS 476.65NT | Aspergillus conjunctus* | ATCC 16796 = IMI 135421 | Forest soil, Palmar, Province of Puntarenas, Costa Rica | JN121688 | JN121523 | JN121829 | JN121920 |
| CBS 553.77T | Aspergillus coremiiformis* | ATCC 38576 = 223069 | Soil, Ivory Coast | JN121700 | JN12153 | JN121839 | JN121926 |
| CBS 656.73NT | Aspergillus egyptiacus* | IMI 141415 | Sandy soil, under Olea europaea (olive tree), Mediterranean Coast, Ras-el-Hikma, Egypt | JN121713 | JN121546 | JN121852 | JN121937 |
| CBS 128202 | Aspergillus flavus1* | NRRL 3357 (= ATCC 200026) | Peanut cotyledons, USA | Unpublished | |||
| Aspergillus fumigatus1* | Af293 | Patient with invasive aspergillosis | Nierman et al. (2005) | ||||
| CBS 116.56NT | Aspergillus funiculosus* | ATCC 16846 = IMI 054397 = IMI 054397ii | Soil, Ibadan, Nigeria | JN121572 | JN121431 | JN121738 | JN121883 |
| CBS 118.45T | Aspergillus janus* | ATCC 16835 = IMI 016065 = IMI 016065ii = MUCL 31307 = NRRL 1787 | Soil, Panama | JN121576 | JN121435 | JN121742 | JN121885 |
| CBS 538.65NT | Aspergillus kanagawaensis* | ATCC 16143 = IMI 126690 | Forest soil under Pinus banksiana, Wisconsin, USA | JN121698 | JN121531 | JN121837 | JN121925 |
| CBS 151.66T | Aspergillus leporis* | ATCC 16490 | Dung of Lepus townsendii (white-tailed Jackrabbit ), near Saratoga, Wyoming, USA | JN121589 | JN121446 | JN121753 | JN121893 |
| CBS 513.88 | Aspergillus niger1* | Derived from NRRL 3122 and currently used as enzyme production strain. | Pel et al. (2007) | ||||
| CBS 101887 | Aspergillus ochraceoroseus* | ATCC 42001 = IBT 14580 | Soil, Tai National Forest, Ivory Coast | JN121557 | JN121416 | JN121723 | JN121871 |
| CBS 108.08NT | Aspergillus ochraceus* | ATCC 1008 = CBS 547.65 = IMI 016247 = IMI 016247iii = IMI 016247iv = NRRL 1642 = NRRL 398 | Unknown source | JN121562 | JN121421 | JN121728 | JN121875 |
| CBS 622.67T | Aspergillus penicilliformis* | ATCC 18328 = IMI 129968= IMI 132431 | Soil under Nicotiana tabacum, Moldavia, Romania | JN121708 | JN121542 | JN121848 | JN121934 |
| CBS 130294 | Aspergillus penicillioides* | DTO 11C3 | Indoor environment, Germany | JN121578 | JN121437 | JN121744 | JN121886 |
| CBS 578.65NT | Aspergillus pulvinus* | ATCC 16842 = IMI 139628 | Forest soil, Liberia, Province of Guanacaste, Costa Rica | JN121703 | JN121536 | JN121842 | JN121930 |
| CBS 117.33NT | Aspergillus restrictus* | ATCC 16912 = CBS 541.65 = IMI 016267 = MUCL 31313 = NRRL 154 = NRRL 4155 | Cloth, UK | JN121574 | JN121432 | JN121740 | JN121884 |
| CBS 649.93T | Aspergillus robustus* | CBS 428.77 = IBT 14305 | Surface soil from thorn-forest, near Mombasa, Kenya | JN121711 | JN121544 | JN121850 | JN121935 |
| CBS 139.61NT | Aspergillus sparsus* | ATCC 16851 = IMI 019394 = IMI 019394ii = MUCL 31314 = NRRL 1933 | Soil, Costa Rica | JN121586 | JN121444 | JN121751 | JN121891 |
| CBS 112812T | Aspergillus steynii* | IBT 23096 | Dried arabica green coffee bean, on parchment, internal infection, Chamumdeshuran Estata, Karnataka, district Giris, India | JN121569 | JN121428 | JN121735 | JN121880 |
| CBS 264.81 | Aspergillus sydowii* | Grains and milling fractions, Triticum aestivum, India | JN121624 | JN121476 | JN121782 | JN121902 | |
| Aspergillus terreus1* | NIH 2624 | Clinical isolate | Unpublished | ||||
| CBS 272.89 | Aspergillus togoensis* | NRRL 13550 | Seed, near La Maboké, Central African Republic | JN121627 | JN121480 | JN121785 | JN121904 |
| CBS 245.65 | Aspergillus versicolor* | ATCC 11730 = ATCC 16020= IMI 045554 = IMI 045554ii = IMI 045554iii = IMI 045554iv = MUCL 19008 | Cellophane, Indiana, USA | JN121614 | JN121468 | JN121775 | JN121899 |
| CBS 104.07NT | Aspergillus wentii* | ATCC 1023 = IMI 017295 = IMI 017295ii = NRRL 1269 = NRRL 375 | Soybeans, Java, Indonesia | JN121559 | JN121418 | JN121725 | JN121873 |
| CBS 506.65NT | Aspergillus zonatus* | ATCC 16867 = IMI 124936 | Forest soil, Province of Linon, Fortuna, Costa Rica | JN121691 | JN121526 | JN121832 | JN121921 |
| CBS 380.74T | Basipetospora halophilica* | IFO 9650 | Undaria pinnatifida (Wakame), Osaka, Japan | JN121666 | JN121509 | JN121815 | JN121910 |
| CBS 100.11NT | Byssochlamys nivea* | ATCC 22260 | Unknown source | JN121511 | JF417414 | JF417381 | JF417514 |
| CBS 101075T | Byssochlamys spectabilis* | ATCC 90900 = FRR 5219 | Heat processed fruit beverage; Tokyo Japan | JN121554 | JF417446 | JF417412 | JF417546 |
| CBS 605.74T | Byssochlamys verrucosa* | ATCC 34163 | Nesting material of Leipoa ocellata (Malleefowl), Pulletop Nature Reserve, New South Wales, Australia | JN680311 | JN121540 | JN121746 | JN121932 |
| CBS 132.31T | Chrysosporium inops* | IMI 096729 = UAMH 802 | Skin man, Italy | JN121584 | JN121443 | JN121750 | JN121890 |
| Coccidioides immitis1* | Strain “RS” | Vaccine strain - origin unknown | Sharpton et al. (2009) | ||||
| CBS 525.83T | Cristaspora arxii* | ATCC 52744 = FMR 416 | Soil, Tarragona, Spain | JN121695 | JN121529 | JN121835 | JN121924 |
| CBS 157.66NT | Dichotomomyces cejpii* | Orchard soil, near Tiraspol, Moldova | JN121589 | JN121447 | JN121754 | JN121894 | |
| Emericella nidulans1* | FGSC A4 (= ATCC 38163 = CBS 112.46) | Unknown source | Galagan et al. (2005) | ||||
| CBS 229.60T | Eupenicillium hirayamae* | ATCC 18312 = IMI 078255 = IMI 078255ii = NRRL 143 | Milled rice, Thailand | JN121604 | JN121459 | JN121766 | JN121946 |
| CBS 518.65NT | Eurotium amstelodami* | ATCC 16464 = IMI 229971 = NRRL 90 | Unknown substrate | JN121694 | JN121528 | JN121834 | JN121923 |
| CBS 516.65NT | Eurotium herbariorum* | ATCC 16469 = IMI 211383 = NRRL 116 | Unpainted board, Washington, USA | JN121693 | JN121527 | JN121833 | JN121922 |
| CBS 260.73T | Fennellia flavipes* | ATCC 24484 = IMI 171883 = NRRL 5504 | Cellulose material buried in forest soil, Pak Thong Chai, Thailand | JN121623 | JN121475 | JN121781 | JN121901 |
| CBS 252.87T | Geosmithia viridis* | IMI 288716 | Soil; bank of creek flowing into Little River; New South Wales; Australia | JN121620 | JF417422 | JF417389 | JF417522 |
| CBS 295.48IsoT | Hamigera avellanea* | ATCC 10414 = IMI 040230 = NRRL 1938 | Soil; San Antonio, Texas, USA | JN121632 | JF417424 | JF417391 | JF417524 |
| CBS 377.48NT | Hamigera striata* | ATCC 10501 IMI 039741 = NRRL 717 | Canned blueberries, USA | JN121665 | JN121508 | JN121814 | JN121909 |
| CBS 527.65T | Hemicarpenteles paradoxus* | ATCC 16918 = IMI 061446 = NRRL 2162 | Dung of Opossum, Wellington, New Zealand | JN121696 | JN121530 | JN121836 | JN121989 |
| CBS 607.74T | Leiothecium ellipsoideum* | ATCC 32453 | Soil, between rocks, Mystras, Peloponnesos, Greece | JN121707 | JN121541 | JN121847 | JN121933 |
| CBS 109402T | Monascus argentinensis* | FMR 7393 | Soil sample, El Infiernillo, Tafi del Valle, Tucumán province, Argentina | JN121564 | JN121423 | JN121730 | JN121877 |
| CBS 113675 | Monascus lunisporas* | FMR 6679 | Soil sample, Corcovado Mountain, Tijuca National Park, Rio de Janeiro, Brazil | JN121570 | JN121429 | JN121736 | JN121881 |
| CBS 109.07T | Monascus purpureus* | ATCC 16365 = ATCC 16426 = IMI210765 = NRRL 1596 | Fermented rice grain, ‘ang-quac’ (purple coloured rice), Kagok-Tegal, imported from China, Prov. Quouan-toung, Java, Indonesia | JN121563 | JN121422 | JN121729 | JN121876 |
| CBS 558.71T | Neocarpenteles acanthosporum* | ATCC 22931 = IMI 164621 | Soil, Bougainville Island, Solomon Islands | JN121701 | JN121534 | JN121840 | JN121928 |
| Neosartorya fischeri* | NRRL 181 | Canned fruit | |||||
| CBS 350.66T | Paecilomyces aerugineus* | IMI 105412 | Debris of Glyceria maxima, Attenborough, Notts., UK | JN121657 | JN121502 | JN121808 | JN121907 |
| CBS 761.68 | Penicilliopsis clavariiformis* | CSIR 1135 | Unknown source, Pretoria, South Africa | JN121716 | JN121549 | JN121855 | JN121940 |
| CBS 246.67HT | Penicillium abidjanum** | ATCC 18385 = FRR 1156 = IMI 136244 | Savannah soil, near Abidjan, Ivory Coast | JN121615 | JN121469 | JN121777 | JN121954 |
| CBS 209.28LT | Penicillium adametzii* | ATCC 10407 = IMI 039751 = MUCL 29106 = NRRL 737 | Soil under conifers, Poznan, Poland | JN121598 | JN121455 | JN121762 | JN121944 |
| CBS 317.67HT | Penicillium alutaceum** | ATCC 18542 = FRR 1158 = IFO 31728 = IMI 136243 | Soil, near Pretoria, South Africa | JN121641 | JN121489 | JN121795 | JN121968 |
| CBS 220.66IsoT | Penicillium arenicola* | ATCC 18321 = ATCC 18330 = IMI117658 = NRRL 3392 | Soil from pine forest, Kiev, Ukraine | JN121601 | JN121457 | JN121764 | JN121897 |
| CBS 241.56NT | Penicillium atrovenetum** | ATCC 13352 = FRR 2571 = IFO 8138 = IMI 061837 | Soil, Sussex Downs, England | JN121614 | JN121467 | JN121774 | JN121953 |
| CBS 299.48AUT | Penicillium camemberti** | ATCC 1105 = ATCC 4845 = FRR 878 = IBT 21508 = IMI 027831 = IMI 092200 = MUCL 29790 = NRRL 877 = NRRL 878 | French Camembert cheese, Connecticut, USA | JN121635 | JN121484 | JN121790 | JN121963 |
| CBS 300.48NT | Penicillium canescens* | ATCC 10419 = IMI 028260 = MUCL 29169 = NRRL 910 | Soil, England | JN121636 | JN121485 | JN121791 | JN121964 |
| CBS 233.81 | Penicillium caperatum | FRR 71 = IMI 216895 | Neotype of E. brefeldianum; soil, Murrumbidgee Irrigation Area, N.S.W., Australia | JN121610 | JN121465 | JN121772 | JN121952 |
| CBS 352.67HT | Penicillium catenatum* | ATCC 18543 = IMI 136241 | Desert soil, Upington, Cape Province, South Africa | JN121659 | JN121504 | JN121810 | JN121980 |
| CBS 304.48T | Penicillium charlesii* | ATCC 8730 = CBS 342.51 = IMI 040232 = NRRL 1887 = NRRL 778 | Unknown source, UK | JN121637 | JN121486 | JN121792 | JN121965 |
| CBS 306.48NT | Penicillium chrysogenum** | ATCC 10106 = FRR 807 = IBT 5233 = IMI 024314 = IMI 092208 = MUCL 29079 = MUCL 29145 = NRRL 807 = NRRL 810 | Cheese, Storrs, Connecticut | JN121638 | JN121487 | JN121793 | JN121966 |
| Penicillium chrysogenum1* | Wisconsin 54-1255 | Moldy cantaloupe Peoria, Illinois, USA | van den Berg et al. (2008) | ||||
| CBS 490.66 | Penicillium cinnamopurpureum* | ATCC 18337 = IMI 114483 | Type of E. cinnamopurpureum; cultivated soil, South Africa | JN121690 | JN121525 | JN121831 | JN121988 |
| CBS 258.29NT | Penicillium citreonigrum* | ATCC 48736 = 092209 = MUCL 28648 = MUCL 29062 = MUCL 29116 = NRRL 761 | Rotting stem, Belgium | JN121622 | JN121474 | JN121780 | JN121957 |
| CBS 139.45NT | Penicillium citrinum* | ATCC 1109 = IMI 091961 = MUCL 29781 = NRRL 1841 | Unknown | JN121585 | JF417416 | JF417383 | JF417516 |
| CBS 232.38 | Penicillium citrinum** | Thom 4733.73 | Type of P. implicatum; unknown source, Belgium | JN121608 | JN121463 | JN121770 | JN121950 |
| CBS 119387T | Penicillium coffeae* | IBT 27866 = NRRL 35363 | Peduncle, Coffea arabica, Oahu, Aiea, Hawaii, USA | JN121577 | JN121436 | JN121743 | JN121862 |
| CBS 231.38 | Penicillium corylophilum** | ATCC 10452 = IFO 7726 = IMI 039817 = NRRL 872 | Type of P. humuli; Humus lupulus (hops), Weihenstephan, Germany | JN121606 | JN121461 | JN121768 | JN121948 |
| CBS 271.89HT | Penicillium cryptum* | ATCC 60138 = IMI 296794 = NRRL 13460 | Soil from Quercus-Betula forest, Hempstead Lake State Park, Long Island, New York | JN121626 | JN121478 | JN121784 | JN121958 |
| CBS 660.80T | Penicillium dendriticum* | IMI 216897 | Leaf litter of Eucalyptus pauciflora, Kosciusko National Park, New South Wales, Australia | JN121714 | JN121547 | JN121853 | JN121938 |
| CBS 112082epiT | Penicillium digitatum** | IBT 13068 | Citrus limon, Italy | JN121567 | JN121426 | JN121733 | JN121858 |
| CBS 456.70T | Penicillium dimorphosporum* | ATCC 22783 = ATCC 52501 = FRR 1120 = IMI 149680 | Mangrove swamp soil, below high tide level, Tooraddin, Westernport Bay, Sawtell's Inlet, Victoria, Australia | JN121683 | JN121517 | JN121823 | JN121985 |
| CBS 322.48AUT | Penicillium duclauxii* | ATCC 10439 = IMI 040044 = MUCL 28672 = MUCL 29094 = MUCL 29212 = NRRL 1030 | Canvas, France | JN121643 | JN121491 | JN121797 | JN121905 |
| CBS 112493T | Penicillium ellipsoideosporum** | AS 3.5688 | Banyan seeds, Pingxiang, Guanbxi Province, China (data after Wang et al. 2007) | JN121568 | JN121427 | JN121734 | JN121859 |
| CBS 318.67HT | Penicillium erubescens** | ATCC 18544 = FRR 814 = IFO 31734 = IMI 136204 | Nursery soil, Pretoria, South Africa | JN121642 | JN121490 | JN121796 | JN121969 |
| CBS 323.71NT | Penicillium euglaucum* | Soil, Argentina | JN121644 | JN121492 | JN121798 | JN121970 | |
| CBS 325.48 | Penicillium expansum* | ATCC 7861 = IBT 5101 = IMI 039761= MUCL 29192 = NRRL 976 | Fruit of Malus sylvestris; USA | JN121645 | JF417427 | JF417394 | JF417527 |
| CBS 229.81NT | Penicillium fellutanum** | ATCC 10443 = CBS 326.48 = FRR 746 = IFO 5761 = IMI 039734 = IMI 039734iii = NRRL 746 | Unknown source, USA | JN121605 | JN121460 | JN121767 | JN121947 |
| CBS 124.68T | Penicillium fractum* | ATCC 18567 = FRR 3448 = IMI 136701 = NRRL 3448 | Soil, Univ. Shinshu, Ueda-shi, Nagano Pref, Japan | JN121582 | JN121441 | JN121748 | JN121864 |
| CBS 295.62NT | Penicillium fuscum** | ATCC 14770 = IFO 7743 = IMI 094209 = MUCL 31196 = NRRL 3008 = WSF 15c | Type of E. pinetorum and neotype of Citromyces fuscus; pine-birch forest soil, Vilas County, Wisconsin, USA | JN121633 | JN121483 | JN121789 | JN121962 |
| CBS 125543NT | Penicillium glabrum* | IBT 22658 = IMI 91944 | Unknown | JN121717 | JF417447 | JF417413 | JF417547 |
| CBS 599.73T | Penicillium gracilentum* | ATCC 28047 = ATCC 48258 = IMI 216900 | Soil, Brown River, Port Moresby, Central Dist., Papua New Guinea | JN121704 | JN121537 | JN121843 | JN121990 |
| CBS 185.27NT | Penicillium griseofulvum* | ATCC 11885 = IBT 6740 = IMI 075832 = IMI 075832ii = MUCL 28643 = NRRL 2152 = NRRL 2300 | Unknown source, Belgium | JN121592 | JN121449 | JN121756 | JN121865 |
| CBS 277.58T | Penicillium griseolum* | ATCC 18239 = IMI 071626 = NRRL 2671 | Acidic dune sand, Dorset, Stufland, England | JN121629 | JN121480 | JN121786 | JN121959 |
| CBS 336.48NT | Penicillium herquei** | ATCC 10118 = FRR 1040 = IFO 31747 = IMI 028809 = MUCL 29213 = NRRL 1040 | Leaf, France | JN121647 | JN121494 | JN121800 | JN121972 |
| CBS 341.68T | Penicillium idahoense* | ATCC 22055 = IMI 148393 | Soil, Latàh Co., Univ. of Idaho Plant Science Farm, Idaho, USA | JN121652 | JN121499 | JN121805 | JN121976 |
| CBS 351.67T | Penicillium inusitatum* | ATCC 18622 = IMI 136214 | Forest soil, Knysna Valley, Cape Province, South Africa | JN121658 | JN121503 | JN121809 | JN121979 |
| CBS 247.56NT | Penicillium isariiforme* | ATCC 18425 = IMI 060371 = MUCL 31191 MUCL 31323 = NRRL 2638 | Woodland soil, Zaire | JN121616 | JN121470 | JN121720 | JN121993 |
| CBS 338.48NT | Penicillium islandicum* | ATCC 10127 = IMI 040042 = MUCL 31324 = NRRL 1036 | Unknown source, Cape Town, South Africa | JN121648 | JN121495 | JN121801 | JN121906 |
| CBS 339.48NT | Penicillium italicum** | ATCC 10454 = FRR 983 = IBT 23029 = IMI 039760 = MUCL 15608 = NRRL 983 | Fruit, Citrus Experiment Station, Riverside, California, USA | JN121649 | JN121496 | JN121802 | JN121973 |
| CBS 340.48NT | Penicillium janthinellum* | ATCC 10455 = IMI 040238 = NRRL 2016 | Soil, Nicaragua | JN131650 | JN121497 | JN121803 | JN121974 |
| CBS 341.48T | Penicillium javanicum* | ATCC 9099 = FRR 707 = IMI 039733 = MUCL 29099 = NRRL 707 | Type of P. javanicum, E. javanicum and P. indonesiae; root of Camellia sinensis (green tea), Buitenzorg, Java, Indonesia | JN121651 | JN121498 | JN121804 | JN121975 |
| CBS 247.67T | Penicillium katangense* | ATCC 18388 = IMI 136206 = NRRL 5182 | Soil, Katanga, Zaire | JN121618 | JN121471 | JN121777 | JN121955 |
| CBS 344.61T | Penicillium kewense* | ATCC 18240 = IMI 086561= MUCL 2685 = NRRL 3332 | Culture contaminant of mineral oil, Kew, Surrey, England, UK | JN121654 | JF417428 | JF417395 | JF417528 |
| CBS 106.11NT | Penicillium lanosum* | ATCC 10458 = IMI 040224 = MUCL 29232 = NRRL 2009 | Unknown source, Germany | JN121561 | JN121420 | JN121727 | JN121857 |
| CBS 343.48T | Penicillium lapidosum* | ATCC 10462 = IMI 039743 = NRRL 718 | Canned blueberry, Washington, USA | JN121653 | JN121500 | JN121806 | JN121977 |
| CBS 277.70T | Penicillium lassenii* | ATCC 22054 = IMI 148395 | Soil under conifers, Tehama Co., Lassen National Forest, 1300 m alt., California, USA | JN121630 | JN121481 | JN121787 | JN121960 |
| CBS 116871T | Penicillium macrosclerotiorum* | AS 3.6581 | Soil, Chongqing, Wushan County, Sichuang Province, China | JN121573 | JN121432 | 121739 | JN121860 |
| CBS 647.95HT | Penicillium malachiteum* | IBT 17515 | Soil, Nihondaira Pref. Park, Shimizu-shi, Shimizu-ken, Japan | JN121710 | JN121543 | JN121849 | JN121991 |
| Penicillium marneffei1* | ATCC 18224 (CBS 334.59 = IMI 68794) | Bamboo rat (Rhizomys sinensis); Vietnam | Unpublished | ||||
| CBS 256.55NT | Penicillium megasporum* | ATCC 12322 = IMI 216904 = NRRL 2232 | Heath soil,Suffolk, England | JN121621 | JN121473 | JN121779 | JN121900 |
| CBS 642.68NT | Penicillium minioluteum* | IMI 089377 = MUCL 28666 | Unknown | JN121709 | JF417443 | JF417409 | JF417543 |
| CBS 353.48NT | Penicillium namyslowskii* | ATCC 11127 = IMI 040033 = MUCL 29226 = NRRL 1070 | Soil under Pinus sp.; Puszcza Bialowieska, Poland | JN121660 | JF417430 | JF417397 | JF417530 |
| CBS 203.84HT | Penicillium nepalense** | NHL 6482 | Rice soil, Boudha, Kathmandu, Nepal | JN121596 | JN121453 | JN121760 | JN121868 |
| CBS 489.66T | Penicillium ochrosalmoneum* | ATCC 18338 = IMI 116248ii | Type of E. ochrosalmoneum; cornmeal, South Africa | JN121689 | JN121524 | JN121830 | JN121987 |
| CBS 232.60NT | Penicillium olsonii* | IBT 23473 = IMI 192502 | Root, Picea abies, alt. 1980 m., Pitztal, Austria | JN121609 | JN121464 | JN121771 | JN121952 |
| CBS 190.68T | Penicillium ornatum* | ATCC 18608 = IMI 137977 = NRRL 3471 | Soil, Moto-machi, Oshima Islands, Japan | JN121594 | JN121451 | JN121758 | JN121867 |
| CBS 462.72HT | Penicillium osmophilum** | IBT 14679 | Agricultural soil, Wageningen, the Netherlands | JN121683 | JN121518 | JN121824 | JN121986 |
| CBS 219.30NT | Penicillium oxalicum** | ATCC 1126 = FRR 787 = IMI 192332 = MUCL 29047 = NRRL 787 | Soil, Connecticut | JN121600 | JN121456 | JN131763 | JN121944 |
| CBS 251.56T | Penicillium ramusculum* | ATCC 12292 = IMI 063546 = NRRL 3459 | Culture contaminant, Brazil | JN121620 | JN121472 | JN121778 | JN121956 |
| CBS 367.48NT | Penicillium restrictum** | ATCC 11257 = FRR 1748 = IMI 040228 = NRRL 1748 | Soil, Honduras | JN121662 | JN121506 | JN121812 | JN121981 |
| CBS 231.61NT | Penicillium sacculum (syn. Eladia saccula)* | ATCC 18350 = IMI 051498 | Soil, Madrid, Spain | JN121607 | JN121462 | JN121769 | JN121949 |
| CBS 122276T | Penicillium saturniforme** | AS 3.6886 | Soil, Jiling Province, China | JN121580 | JN121439 | JN121746 | JN121863 |
| CBS 290.48T | Penicillium shearii* | ATCC 10410 = IMI 039739 = IMI 039739iv = NRRL 715 | Soil, Tela, Honduras | JN121631 | JN121482 | JN121788 | JN121961 |
| CBS 228.89T | Penicillium shennangjianum** | AS 3.4526 | Mouldy pea, Hubei Province, Shennongjia, China | JN121603 | JN121458 | JN121766 | JN121945 |
| CBS 372.48NT | Penicillium simplicissimum* | ATCC 10495 = IFO 5762 = IMI 039816 | Flannel bag, Cape, South Africa | JN121662 | JN121507 | JN121813 | JN121981 |
| CBS 315.67T | Penicillium stolkiae* | ATCC 18546 = IMI 136210 | Peaty forest soil, Eastern Transvaal, South Africa | JN121640 | JN121488 | JN121794 | JN121967 |
| CBS 117503T | Penicillium thiersii* | IBT 27050 = NRRL 28162 | Old, black stroma, encrusting the surface of dead Acer saccharum log, alt. 300 m., New Glarus Woods State Park, Wisconsin, USA | JN121575 | JN121434 | JN121741 | JN121861 |
| CBS 347.59 | Penicillium thomii** | IFO 6031 = IMI 068221 | Type of P. thomii var. flavescens; soil, Japan | JN121655 | JN121501 | JN121807 | JN121978 |
| CBS 430.69T | Penicillium tularense* | ATCC 22056 = IMI 148394 | Soil, under Pinus ponderosa and Quercus kelloggii, Tulare Co., Pine Flat, California | JN121681 | JN121516 | JN121822 | JN121984 |
| CBS 603.74NT | Penicillium verrucosum** | ATCC 48957 = FRR 965 = IBT 12809 = IBT 4733 = IMI 200310 = IMI 200310ii = MUCL 28674 = MUCL 29089 = MUCL 29186 = NRRL 965 | Unknown source, Belgium | JN121706 | JN121539 | JN121845 | JN121991 |
| CBS 390.48NT | Penicillium viridicatum** | ATCC 10515= IBT 23041 = IMI 039758 = IMI 039758ii = NRRL 963 | Air, District of Columbia, Washington D.C., USA | JN121668 | JN121511 | JN121817 | JN121983 |
| CBS 430.64IsoT | Phialomyces macrosporus* | ATCC 16661 = IMI 110130 = MUCL 9776 | Soil, near Rotorua, New Zealand | JN121680 | JN121515 | JN121821 | JN121915 |
| CBS 128032T | Phialosimplex caninus* | UAMH 10337 | Bone marrow aspirate ex dog, San Antonio, Texas, USA | JN121587 | JN121445 | JN121752 | JN121892 |
| CBS 109945T | Phialosimplex chlamydosporus* | FMR 7371 = IMI 387422 | Disseminated infection in a dog | JN121566 | JN121425 | JN121732 | JN121879 |
| CBS 366.77T | Phialosimplex sclerotialis* | IAM 14794 | Fodder of ray-grass and lucerne, France | JN121661 | JN121505 | JN121811 | JN121908 |
| CBS 384.61T | Polypaecilum insolitum* | ATCC 18164 = IMI 075202 = MUCL 3078 | Ear of human, Leeds, Yorkshire, England, UK | JN121667 | JN121510 | JN121816 | JN121911 |
| CBS 101166 | Polypaecilum pisci* | Yeast extract, Netherlands | JN121555 | JN121415 | JN121722 | JN121870 | |
| CBS 101.69T | Rasamsonia argillacea* | DTO 97E4 = IMI 156096 = IBT 31199 | Mine tip with a very high surface temperature; Staffordshire, UK | JN121556 | JF417415 | JF417382 | JF417515 |
| CBS 413.71T | Rasamsonia byssochlamydoides* | DTO 149D6 = IBT 11604 | Dry soil under Douglas fir; Oregon, USA | JN121675 | JF417437 | JF417403 | JF417537 |
| CBS 275.58NT | Rasamsonia cylindrospora* | DTO 138F8 = IBT 31202 = ATCC 18223 = IMI 071623 | Culture contaminant; Berkshire, England, UK | JN121628 | JF417423 | JF417390 | JF417523 |
| CBS 393.64T | Rasamsonia emersonii* | DTO 48I1 = IBT 21695 = ATCC 16479 = IMI 116815 = IMI 116815ii | Compost; Italy | JN121670 | JF417434 | JF417401 | JF417534 |
| CBS 114.72IsoT | Sagenoma viride* | ATCC 22467 = NRRL 5575 | Soil, Australia | JN121571 | JN121430 | JN121737 | JN121882 |
| CBS 545.86T | Sagenomella bohemica* | CCF 2330 = IAM 14789 | Peloids for balneological purposes, Frantiskovy Lázne Spa, West Bohemia, Czech Republic | JN121699 | JN121532 | JN121838 | JN121927 |
| CBS 398.69 | Sagenomella diversispora* | Forest soil under Populus tremuloides; Petawawa, Ontario, Canada | JN121673 | JF417435 | JF417402 | JF417536 | |
| CBS 399.69 | Sagenomella diversispora* | MUCL 15012 | Forest soil under Thuja occidentalis, Aberfoyle, Ontario, Canada | JN121674 | JN121513 | JN121819 | JN121913 |
| CBS 426.67 | Sagenomella griseoviridis* | ATCC 18505 = IMI 113160 | Unknown source | JN121677 | JF417438 | JF417404 | JF417538 |
| CBS 427.67IsoT | Sagenomella humicola* | ATCC 18506 = IMI 113166 | Forest soil under Thuja occidentalis; Ontario, Canada | JN121678 | JF417439 | JF417405 | JF417539 |
| CBS 429.67IsoT | Sagenomella striatispora* | ATCC 18510 = IMI 113163 | Soil; Guelph, Ontario, Canada | JN121679 | JF417440 | JF417406 | JF417540 |
| CBS 414.78T | Sagenomella verticillata* | IAM 14697 | Conifer forest soil, Sweden | JN121676 | JN121514 | JN121820 | JN121914 |
| CBS 124.53NT | Sclerocleista ornata* | ATCC 16921 = IMI 055295 = MUCL 15643 = NRRL 2256 | Soil in oak forest, Dane Co., Madison, Wisconsin, USA | JN121581 | JN121440 | JN121747 | JN121888 |
| CBS 105.25 | Sclerocleista thaxteri* | IMI 055296 = NRRL 2292 | Dung of caterpillar, USA | JN121560 | JN121419 | JN121726 | JN121874 |
| CBS 296.48T | Talaromyces bacillisporus* | ATCC 10126 = IMI 040045 = NRRL 1025 | Begonia leaf; New York City, New York, USA | JN121634 | JF417425 | JF417392 | JF417525 |
| CBS 100537T | Talaromyces convolutus* | IBT 14989 | Soil, Kathmandu, Nepal | JN121553 | JN121414 | JN121721 | JN121869 |
| CBS 100536T | Talaromyces emodensis* | IBT 14990 | Soil; Kathmandu, Nepal | JN121552 | JF417445 | JF417411 | JF417545 |
| CBS 310.38NT | Talaromyces flavus* | IMI 197477 = NRRL 2098 | Unknown substrate; New Zealand | JN121639 | JF417426 | JF417393 | JF417526 |
| CBS 398.68T | Talaromyces leycettanus* | ATCC 22469 = IMI 178525 | Coal spoil tip soil; Leycett, Staffordshire, England, UK | JN121672 | JF417435 | JF417402 | JF417535 |
| CBS 348.51NT | Talaromyces luteus* | IMI 089305 | Soil, UK | JN121656 | JF417429 | JF417396 | JF417529 |
| CBS 475.71IsoT | Talaromyces purpureus* | ATCC 24069 = ATCC 52513 = FRR 1731 = IMI 181546 | Soil, near Esterel, France | JN121687 | JN121522 | JN121828 | JN121919 |
| Talaromyces stipitatus1* | ATCC 10500 (= NRRL 1006 = CBS 375.48 = IMI 39805) | Rotting wood; Louisiana, USA | Unpublished | ||||
| CBS 236.58T | Talaromyces thermophilus* | ATCC 10518 = IMI 048593 = NRRL 2155 | Parthenium argentatum, decaying plant; California, USA | JN121611 | JF417420 | JF417387 | JF417520 |
| CBS 373.48T | Talaromyces trachyspermus* | ATCC 10497 = IMI 040043 = NRRL 1028 | Unknown source, USA | JN121664 | JF417432 | JF417399 | JF4174532 |
| CBS 391.48NT | Talaromyces wortmanii* | ATCC 10517 = IMI 040047 = NRRL 1017 | Unknown source | JN121669 | JF417433 | JF417400 | JF417533 |
| CBS 891.70 | Thermoascus aurantiacus* | IMI 173037 | Wood; Firenze, Italy | JN121719 | JF417444 | JF417410 | JF417544 |
| CBS 396.78 | Thermoascus aurantiacus* | JCM 12816 | Sawdust, in lumber yard, Toronto, Ontario, Canada | JN121671 | JN121512 | JN121818 | JN121912 |
| CBS 181.67T | Thermoascus crustaceus* | ATCC 16462 = IMI 126333 | Parthenium argentatum, decaying plant; Salinas, California, USA | JN121591 | JF417417 | JF417384 | JF417517 |
| CBS 528.71NT | Thermoascus themophilus* | IMI 123298 = NRRL 5208 | Wood and bark of Pinus; Sweden | JN121697 | JF417442 | JF417408 | JF417542 |
| CBS 218.34 | Thermomyces lanuginosus* | MUCL 8338 | Fruit shell of Theobroma cacao | JN121599 | JF417418 | JF417385 | JF417518 |
| CBS 224.63 | Thermomyces lanuginosus* | MUCL 8337 | Mushroom compost; Gossau-Zürich Switzerland | JN121602 | JF417419 | JF417386 | JF417519 |
| CBS 334.68T | Thysanophora canadensis* | ATCC 18741 = IMI 137644 = MUCL 21216 | Needle of Tsuga canadensis, Bell's Corners, Ontario, Canada | JN121647 | JN121493 | JN121799 | JN121971 |
| CBS 206.57T | Thysanophora taxi* | ATCC 18484 = MUCL 11402 | Litter, Berlin, Germany | JN121597 | JN121454 | JN121761 | JN121942 |
| CBS 185.65 | Torulomyces lagena* | MUCL 8221 | Bog soil under Thuja plicata, Guelph, Ontario, Canada | JN121593 | JN121450 | JN121757 | JN121866 |
| CBS 247.57 | Trichocoma paradoxa* | MUCL 39666 = IBT 31159 | Unknown source; Hachijô, Japan | JN121617 | JF417421 | JF417388 | JF417521 |
| CBS 103.73 | Trichocoma paradoxa* | Unknown source, Japan | JN121558 | JN121417 | JN121724 | JN121872 | |
| CBS 788.83 | Trichocoma paradoxa* | Rotting stump of cut down tree, Myojoji Temple near Hakui Noto Park, Ishikawa Pref., Japan | JN121718 | JN121550 | JN121856 | JN121941 | |
| CBS 512.65NT | Warcupiella spinulosa* | ATCC 16919 = IMI 075885 = NRRL 4376 | Jungle soil; Berakas-Muara, Brunei | JN121692 | JF417441 | JF417407 | JF417541 |
| CBS 236.71T | Xeromyces bisporus*1 | IMI 063718 | Mouldy stick of liquorice, Homebush, New South Wales, Australia | JN121612 | JN121466 | JN121773 | JN121898 |
DNA extraction, amplification and sequencing
Genomic DNA was extracted using the Ultraclean Microbial DNA isolation kit (MoBio Laboratories, Carlsbad, CA, USA), according to the manufacturer's instructions. Parts of the following loci were amplified and sequenced for the species listed in Table 1: 1. RPB1, RNA polymerase II largest subunit (regions E and F; according Matheny et al. 2002), 2. RPB2, RNA polymerase II second largest subunit (regions 5–7), 3. Cct8, subunit of the cytosolic chaperonin Cct ring complex, related to Tcp1p and required for the assembly of actin and tubulins in vivo (Stoldt et al. 1996, Kim et al. 1994), 4. Tsr1, protein required for processing of 20S pre-rRNA in the cytoplasm (Gelperin et al. 2001, Léger-Silvestre et al. 2004). Partial RPB2 data was obtained for the majority of species listed in Table S1. Exceptions are strains used in the study of Houbraken et al. (2011c); in that case, published partial β-tubulin sequences were used.
The RPB1 fragment was amplified using the primer pair RPB1-F1843 and R3096, and RPB1-R2623 was occasionally used as an internal primer for sequencing. A part of the RPB2 locus was amplified using the primer pair RPB2-5F and RPB2-7CR (Liu et al. 1999) or the primer pair RPB2-5F_Eur and RPB2-7CR_Eur. The internal sequencing primers RPB2-F311 and RPB2-R310 were occasionally used when poor results were obtained with the regular forward and reverse primers. Amplification of a part of the Cct8 gene was performed using the primer pair Cct8-F660 and Cct8-R1595. No amplicons could be obtained in the case of 5–10 % of the analysed strains. In those cases, amplicons were generated using the primer pair Cct8-R1595 and Cct8-F94. A part of the Tsr1 gene was amplified using the forward primers Tsr1-F1526Pc or Tsr1-F1526 in combination with Tsr1-R2434. Annealing temperatures and primers used for amplification and sequencing are shown in Table 2.
Table 2
Primers used in this study for amplification and sequencing.
| Locus | Primer | Sequence (5′-3′) | Annealing (°C) | Fragment size (bp) | References |
|---|---|---|---|---|---|
| Cct8 | F94 | (Fwd) CGCAAC AAGATYGTBATYAACCA | 50–52 | F94-R1595: 1400–1450 | Houbraken et al. 2011d |
| F660 | (Fwd) GIGTKGTBAAGATCATGGGWGG | F660-R1595: 850–890 | Houbraken et al. 2011d | ||
| R1595 | (Rev) RTCMACRCCNGTIGTCCAGTA | Houbraken et al. 2011d | |||
| RPB1 | F1843 | (Fwd) ATTTYGAYGGTGAYGARATGAAC | 48–53 | ca. 1000 | This study |
| R3096 | (Rev) GRACRGTDCCRTCATAYTTRACC | This study | |||
| R2623 | GCRTTGTTSARATCCTTMARRCTC | This study | |||
| RPB2 | 5F | GAYGAYMGWGATCAYTTYGG | 48–51 | ca. 1220 | Liu et al. 1999 |
| 7CR | CCCATRGCTTGYTTRCCCAT | Liu et al. 1999 | |||
| 5F_Eur | (Fwd) GAYGAYCGKGAYCAYTTCGG | Houbraken et al. 2011d | |||
| 7CR_Eur | (Rev) CCCATRGCYTGYTTRCCCAT | Houbraken et al. 2011d | |||
| F311 | CATGATYCARCGIAAYATGGA | This study | |||
| R310 | CCATRTTICGYTGRATCATGAA | This study | |||
| Tsr1 | F1526Pc | (Fwd) GARTAYCCBCARTCNGAGATGT | 48–50 | ca. 820 | Houbraken et al. 2011d |
| F1626 | (Fwd) GARTAYCCBCARTCNGAIATGT | This study | |||
| R2434 | (Rev) ASAGYTGVARDGCCTTRAACCA | Houbraken et al. 2011d |
The PCR reactions were performed in 25 μL reaction mixtures containing 1 μL genomic DNA 2.5 μL PCR buffer, 0.75 μL MgCl2 (50 mM), 16.55 μL demineralised sterile water, 1.85 μL dNTP (1 mM), 0.50 μL of each primer (100 mM) and 0.1 μL Taq polymerase (5 U/μL, BioTaq, Bioline). The PCR program typically was: 5 cycles of 30 s denaturation at 94 °C, followed by primer annealing for 30 s at 51 °C, and extension for 1 min at 72 °C; followed by 5 cycles with an annealing temperature at 49 °C and 30 cycles at 47 °C, finalised with an extension for final 10 min at 72 °C. Excess primers and dNTP's were removed from the PCR product using the QIAQuick PCR purification kit (Qiagen). Purified PCR fragments were resuspended in 30–50 μL of water. PCR products were sequenced directly in both directions with the same primers and DYEnamic ET Terminator Cycle Sequencing Kit (Amersham Bioscience, Roosendaal, The Netherlands). The cycle sequencing reaction mixture had a total reaction volume of 10 μL, and contained 1 μL of template DNA, 0.85 μL BigDye reagent, 3 μL buffer, 4.75 μL demineralised water and 0.4 μL primer (10 mM).
Sequencing products were purified according to the manufacturers' recommendations with Sephadex G-50 superfine columns (Amersham Bioscience, Roosendaal, The Netherlands) in a multiscreen HV plate (Millipore, Amsterdam, The Netherlands) and with MicroAmp Optical 96-well reaction plate (AB Applied Biosystems, Nieuwerkerk a/d Yssel, The Netherlands). Contigs were assembled using the forward and reverse sequences with the programme SeqMan from the LaserGene package (DNAStar Inc., Madison, WI).
Phylogenetic analysis
The protein coding nucleotide sequences were translated into amino acid data prior to alignment and subsequently aligned using the Muscle software in the MEGA5 package. After aligning, the amino acid data were translated into nucleotide data and used in the phylogenetic analysis. Combined sequence data sets were used in the study on the phylogeny of Trichocomaceae and Penicillium. Before combining the data sets, each data set was analysed using RAxML (Stamatakis et al. 2008). The number of bootstrap runs was set to 100. The program compat.py (from http://www.lutzonilab.net) was used to detect major topological incongruences among single gene data sets (Kauff & Lutzoni 2002). Conflicts were considered significant when a sequence was differentially resolved between two gene trees with greater than 70 % bootstrap support. If no conflicts were detected, then the data sets were combined.
Statistical support was measured by Maximum Likelihood (ML) analysis using the RAxML (randomised axelerated maximum likelihood) software (Stamakis et al. 2008). The robustness of trees in the ML analyses was evaluated by 1000 bootstrap replications. A second measure for statistical support was performed by Bayesian tree inference (BI) analysis using MrBayes v. 3.1.2 (Ronquist & Huelsenbeck 2003). Prior to analysis, the most suitable substitution model was determined using MrModeltest v. 2.3 (Nylander 2004), utilising the Akaike Information Criterion (AIC). The Bayesian analysis was performed with two sets of four chains (one cold and three heated) and the stoprule option, stopping the analysis at an average standard deviation of split frequencies of 0.01. The sample frequency was set to 100; the first 25 percent of trees were removed as burnin. The phylograms obtained with the RAxML analysis were used for presenting the data. Bootstrap values lower than 70 % were considered unreliable because their wide range of error and Bayesian posterior probabilities are considered unreliable below 0.95 (Murphy et al. 2001, Wilcox et al. 2002, Alfaro & Holder 2006). Therefore, only posterior probability (pp) values higher than 0.95 and bootstrap (bs) values higher than 70 % were plotted on those phylograms. Coccidioides immitis (strain RS), a member of Onygenales, was chosen to root the phylogram used in the study on the relationships of Penicillium species among Trichocomaceae. Penicillium (= Talaromyces) marneffei ATCC 18227T was selected as an outgroup for the analysis of the phylogeny of Penicillium. Various phylograms were prepared for assignment of species to sections. All data sets were based on partial RPB2 sequences and rooted with Talaromyces flavus CBS 310.38NT, with exception of the phylogram of sections Lanata-divaricata and Stolkia, which is based on partial β-tubulin data. Penicillium glabrum CBS 125543T was used as an outgroup.
RESULTS
Phylogeny of Trichocomaceae
A phylogenetic study using four combined loci (RPB1, RPB2, Cct8 and Tsr1) was conducted to determine the relationship among members of Trichocomaceae. A total of 157 species were included in the analysis and the total length of the alignment was 3 111 characters, 1 939 of those characters were variable. The length of the Cct8, Tsr1, RPB1 and RPB2 partitions were 714, 669, 768, 960 base pairs long, respectively. The GTR+I+G model was optimal for all four partitions.
The result of the analysis is shown in Fig. 1 and indicates that Trichocomaceae can be divided into three lineages. Lineage 1 is divided into seven clades (clades 1–7) and these clades are on a well-supported branch (100 % bs, 1.00 pp). The type species of the genera Chromocleista (C. malachitea), Eladia (E. saccula),Eupenicillium (E. crustaceum), Hemicarpenteles (H. paradoxus), Penicillium (P. expansum), Thysanophora (T. penicillioides) and Torulomyces (T. lagena) belong to clade 1. This clade is named Penicillium sensu stricto and is divided into two subclades: clade 1A and 1B. The types of subgenera Aspergilloides and Furcatum are accommodated in clade 1A and the type of subgenus Penicillium belongs to clade 1B. Clade 2 is moderately supported (< 70 % bs, 1.00 pp) and contains the type species of the genera Aspergillus (A. glaucus), Cristaspora (C. arxii), Phialosimplex (P. caninus), Polypaecilum (P. insolitum) and the teleomorphs of Aspergillus (Fennellia, Eurotium, Emericella, Neocarpenteles, Dichotomyces, Neosartorya, Sclerocleista). Not all teleomorph genera of Aspergillus are represented in our analysis; however, previous data has shown the genera Chaetosartorya, Neopetromyces and Petromyces also belong to this lineage (Peterson 2008). This clade is subdivided into six groups. Four of the six groups represent the Aspergillus subgenera as defined by Peterson (2008). In addition, also Aspergillus section Cremei and a clade with Phialosimplex and Polypaecilum are present. Clade 3 comprises the type species of Hamigera (H. avellanea), Warcupiella (W. spinosa) and Raperia (R. spinulosa) but this clade is poorly supported (< 70 % bs, < 0.95 pp). Clade 4 contains P. clavariiformis, the type species Penicilliopsis. The type species of the genera Basipetospora (B. rubra), Fraseriella (F. bisporus), Leiothecium (L. ellipsoideum), Monascus (M. ruber), Xeromyces (X. bisporus) cluster together in clade 5. Phialomyces (P. macrosporus) and Sclerocleista (S. ornata) belong to clade 6 and 7, respectively. Lineage 2 is subdivided into two clades: the type species of Thermoascus, Coonemeria and Dactylomyces belong to clade 8, and the types of the genera Byssochlamys (B. nivea) and Paecilomyces (P. variotii) belong to clade 9. The posterior probability value indicates a strong relationship between these two clades (0.99); however, the maximum likelihood analysis resulted in a bootstrap value lower than 70 % (67 %). The posterior probability and bootstrap values are also contradictory regarding the relationship between lineages 1 and 2 (< 70 % bs, 1.00 pp). Lineage 3 is subdivided into five clades (clades 10–14) and these clades are on a strongly supported branch (100 % bs, 1.00 pp). Clade 10 is centered on the type species of Talaromyces, T. flavus, and the type species of Sagenoma (S. viride) also belongs in this clade. The type species of Thermomyces (T. lanuginosus), Sagenomella (S. diversispora), Rasamsonia (R. emersonii) and Trichocoma (T. paradoxa) belong in clades 11–14, respectively.
Best-scoring Maximum Likelihood tree using RAxML based on combined data set of partial Cct8, Tsr1, RPB1 and RPB2 sequences showing the relationship among members of Trichocomaceae. The BI posterior probabilities (pp) values and bootstrap (bs) percentages of the maximum likelihood (ML) analysis are presented at the nodes (pp/bs). Values less than 50 % supported in the ML or less than 0.90 in the Bayesian analysis are indicated with a hyphen, whereas asterisks indicate full support (100 % bs or 1.00 pp). The branches with more than 95 % bootstrap support and 1.00 posterior probability values are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Coccidioides immitis (strain RS).
Phylogeny of Penicillium sensu stricto
The phylogenetic relationship among members of Penicillium s. str. was studied using the same four combined loci (RPB1, RPB2, Cct8 and Tsr1). In total, 72 strains were included in the analysis and the total length of the alignment was 3 393 characters, and 1 805 of them were variable. Penicillium (= Talaromyces) marneffei was used as an outgroup. The length of the Cct8, Tsr1, RPB1 and RPB2 partitions were 723, 759, 955, 957 base pairs, respectively. The best-fit model GTR+I+G was optimal for all four partitions. The result of the analysis is shown in Fig. 7 and confirms the result above that Penicillium s. str. can be divided into two distinct lineages. Similarly, the type species of subgenus Aspergilloides, P. aurantiobrunneum (= P. glabrum) and Furcatum (P. citrinum), belong to lineage 1 and the type of subgenus Penicillium belongs to lineage 2. Lineage 1 is subdivided in 14 clades (Fig. 7). These clades (1–14) were in most cases supported with a bootstrap value higher than 95 % and a posterior probability of 1.00. Lineage 2 is subdivided into 11 clades (15–25). Clades 20–25 are on well-supported branches; however, the overall bootstrap and posterior probability values of clades 15–19 are low. The numbering of the clades is therefore based on the analysis of the partial β-tubulin data in Samson et al. (2004), because well-supported clades (sections) were present in that phylogenetic treatment. Five separate phylograms (Figs (Figs8,8, ,10,10, ,11,11, ,12,12, ,13)13) were prepared in order to determine which species belong to which clade (section). Details of these analyses are summarised in Table 3.
Best-scoring Maximum Likelihood tree using RAxML based on combined data set of partial Cct8, Tsr1, RPB1 and RPB2 sequences showing the relationship among members of Penicillium s. str. Penicillium s. str. is divided in two lineages (s/g Aspergilloides and Penicillium) and 25 sections. The BI posterior probabilities (pp) values and bootstrap (bs) percentages of the maximum likelihood (ML) analysis are presented at the nodes (bs/pp). Values less than 70 % supported in the ML or less than 0.95 in the Bayesian analysis are indicated with a hyphen, whereas asterisks indicate good support (100 % bs or 1.00 pp). The branches with more than 95 % bootstrap support and 1.00 posterior probability values are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Penicillium (= Talaromyces) marneffei ATCC 18227T.
Best-scoring Maximum Likelihood tree using RAxML based on partial RPB2 sequences and giving an overview of the members accommodated in sections Aspergilloides, Sclerotiora and Charlesii. The BI posterior probabilities (pp) values and bootstrap (bs) percentages of the maximum likelihood (ML) analysis are presented at the nodes (pp/bs). Values less than 70 % supported in the ML or less than 0.95 in the Bayesian analysis are indicated with a hyphen, whereas asterisks indicate good support (100 % bs or 1.00 pp). The branches with more than 95 % bootstrap support and 1.00 posterior probability values are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Talaromyces flavus CBS 310.38NT.
Best-scoring Maximum Likelihood tree using RAxML based on partial RPB2 sequences and giving an overview of the members accommodated in sections Exilicaulis, Cinnamopurpurea, Ramigena and Gracilenta. The BI posterior probabilities (pp) values and bootstrap (bs) percentages of the maximum likelihood (ML) analysis are presented at the nodes (pp/bs). Values less than 70 % supported in the ML or less than 0.95 in the Bayesian analysis are indicated with a hyphen, whereas asterisks indicate good support (100 % bs or 1.00 pp). The branches with more than 95 % bootstrap support and 1.00 posterior probability values are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Talaromyces flavus CBS 310.38NT.
Best-scoring Maximum Likelihood tree using RAxML based on partial β-tubulin sequences and giving an overview of the members accommodated in sections Lanata-divaricata and Stolkia. The BI posterior probabilities (pp) values and bootstrap (bs) percentages of the maximum likelihood (ML) analysis are presented at the nodes (pp/bs). Values less than 70 % supported in the ML or less than 0.95 in the Bayesian analysis are indicated with a hyphen, whereas asterisks indicate good support (100 % bs or 1.00 pp). The branches with more than 95 % bootstrap support and 1.00 posterior probability values are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Penicillium glabrum CBS 125543T.
Best-scoring Maximum Likelihood tree using RAxML based on partial RPB2 sequences and giving an overview of the members accommodated in sections Citrina and Ochrosalmonea. The BI posterior probabilities (pp) values and bootstrap (bs) percentages of the maximum likelihood (ML) analysis are presented at the nodes (pp/bs). Values less than 70 % supported in the ML or less than 0.95 in the Bayesian analysis are indicated with a hyphen, whereas asterisks indicate good support (100 % bs or 1.00 pp). The branches with more than 95 % bootstrap support and 1.00 posterior probability values are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Talaromyces flavus CBS 310.38NT.
Best-scoring Maximum Likelihood tree using RAxML based on partial RPB2 sequences and giving an overview of the members accommodated in subgenus Penicillium (clades 15–25). The BI posterior probabilities (pp) values and bootstrap (bs) percentages of the maximum likelihood (ML) analysis are presented at the nodes (pp/bs). Values less than 70 % supported in the ML or less than 0.95 in the Bayesian analysis are indicated with a hyphen, whereas asterisks indicate good support (100 % bs or 1.00 pp). The branches with more than 95 % bootstrap support and 1.00 posterior probability values are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Talaromyces flavus CBS 310.38NT.
Table 3
Details of each analysis of the data sets used for generating Figs 8, 10–13.
| Figure | Clades, acc. Fig. 7 | Locus | No. isolates | Length alignment | Best-fit model |
|---|---|---|---|---|---|
| 8 | 1, 2, 3 | RPB2 | 50 | 916 | SYM+I+G |
| 10 | 6, 7, 10 and 13 | RPB2 | 69 | 916 | GTR+I+G |
| 11 | 11, 12 | β-tubulin | 45 | 528 | HKY+I+G |
| 12 | 5, 14 | RPB2 | 44 | 849 | SYM+I+G |
| 13 | 15–25 | RPB2 | 86 | 916 | GTR+I+G |
DISCUSSION
Part one: Phylogenetic analysis of Trichocomaceae
Choice of genes
Parts of the RPB1, RPB2, Tsr1 and Cct8 genes were only used for the construction of the phylogenetic relationships among members of Trichocomaceae and Penicillium species, and the ability of these genes for species recognition remains largely unexplored. The regions E and F (according Matheny et al. 2002) of the RPB1 gene were analysed. No additional sequence data of Trichocomaceae were published on this part of the RPB1 gene and comparison with other studies is therefore difficult. The regions 5–7 of the RPB2 gene are commonly used in taxonomic studies of Penicillium and Aspergillus and proved to be a good marker for species recognition (e.g. Peterson 2008, Serra et al. 2008, Peterson & Horn 2009, Peterson et al. 2010, Barreto et al. 2011). However, RPB1 and RPB2, as well as TEF1α, β-tubulin, and γ-actin, were not found among the best performing genes for fungal systematics (Aguileta et al. 2008). Aguileta et al. (2008) studied, using a bioinformatics approach, the performance of single-copy protein-coding genes for fungal phylogenetics. Their analyses of 30 published fungal genomes revealed that MCM7 (= MS456), Tsr1 (= MS277) and Cct8 (= FG610) were among the best single-copy genes in phylogenetic utility. MCM7, the best gene for recovering a larger-scale phylogeny across fungal groups, was excluded in the current study since it was not variable enough within the genus Penicillium (Marthey et al. 2008). Tsr1 and Cct8 were also used in other (phylogenetic) studies of groups belonging to Trichocomaceae (López-Villavicencio et al. 2010, Peterson et al. 2010). Analysis of the Tsr1 gene generated the best resolved trees, when compared with Cct8, MCM7 and ITS (López-Villavicencio et al. 2010). The sequenced parts of the RPB1, RPB2, Tsr1 and Cct8 genes mainly contain exons, and the alignment of these loci is therefore unambiguous. This is the main advantage over ITS regions where alignment above genus can be difficult. Furthermore, the ITS region is generally considered unreliable as a phylogenetic marker, especially above genus rank. β-tubulin and calmodulin sequences are often used in taxonomical studies of Penicillium, Paecilomyces and Aspergillus (e.g. Samson et al. 2004, Houbraken et al. 2007, Samson et al. 2009, Varga et al. 2011). However, a large part of these genes consists of intron data and these regions cannot be aligned above genus level, resulting in loss of information in these data sets. In addition, there is evidence that β-tubulins are present in the genome in multiple copies and thus have the potential of being phylogenetically misleading (Landvik et al. 2001, Peterson 2008).
Phylogenetic analysis of Trichocomaceae
Three lineages are recognised in Trichocomaceae (Fig. 1) and we propose to treat these three lineages as distinct families: Trichocomaceae, Aspergillaceae and Thermoascaceae. Lineage 1 corresponds with Aspergillaceae and this name is the oldest available family name within the analysed group of related genera. Malloch & Cain (1972) did not accept this family name since it was based on the asexual (anamorph) form-genus Aspergillus and therefore not applicable for ascomycete perfect (sexual) states. Because we are applying a single-name system and give priority to the oldest name, the family name Aspergillaceae is re-instated. Phylogenetically, Monascaceae belong to Aspergillaceae and this is in agreement with other studies that show that Monascus (type genus of Monascaceae) is related to Penicillium and/or Aspergillus (Berbee et al. 1995, Ogawa et al. 1997, Ogawa & Sugiyama 2000, Peterson 2008, Pettersson et al. 2011). In contrast, Stchigel et al. (2004), who used ITS sequence data to determine the molecular relationships of Monascaceae taxa, concluded that Monascus and Xeromyces form a well-supported, monophyletic clade (81 % bs), separate from Eurotiales (Stchigel & Guarro 2007). These contradictory results can be explained by a deeper taxon sampling in this study combined with a phylogeny based on sequences of four protein-coding genes instead of ITS sequences alone. The Thermoascaceae (= lineage 2) were introduced by Apinis (1967) and typified by Thermoascus. Lineage 3 corresponds to Trichocomaceae and this family was introduced by Fischer (1897) (as Trichocomataceae) and is typified by Trichocoma. The Eurotiaceae were placed in synonymy with this family because the name Trichocomaceae predates Eurotiaceae (Malloch & Cain 1972). The current analysis shows that Eurotiaceae (type genus Eurotium) should be placed in synonymy with Aspergillaceae. The family names Hemicarpenteleaceae, Penicilliopsidaceae, Phialomycetaeae, Warcupiellaceae, Xeromycetaceae and Talaromycetaceae were introduced by Locquin (1972, 1984) but all lack a Latin description and are invalidly published.
Phenotypic classification and delimitation of Aspergillaceae, Trichocomaceae and Thermoascaceae
Several studies on the classification of Trichocomaceae and Eurotiales based on phenotypic characters were published (Malloch & Cain 1972, Fennell 1973, Benny & Kimbrough 1980, Malloch 1985a, b, von Arx 1987) and an overview of selected studies is shown in Table 4. Some of these classifications differ significantly from each other. We compared the results of these studies with the current proposed phylogenetic classification and this showed that our phylogenetic classification largely corresponds with the phenotypic classification described by Malloch (1985a, b). Malloch (1985a, b) divided Trichocomaceae into two subfamilies, Trichomoideae and Dichlaenoideae, based on phenotypic characters including cleistothecial initials, peridium, ascus structure and ascospore morphology. Malloch's list of genera belonging to Dichlaenoideae largely corresponds with the genera we place in Aspergillaceae and his definition of Trichomoideae is comparable with our phylogenetically defined Trichocomaceae. There are two main differences: a) Monascus is treated here in Aspergillaceae and b) the genera Byssochlamys and Thermoascus are accommodated in Thermoascaceae; these were treated by Malloch (1985a, b) in Trichomoideae and Dichlaenoideae, respectively. Using the characters proposed by Malloch in his classification, Aspergillaceae are characterised by the production of asci inside cleistothecia, stromata, or are surrounded by Hülle cells and mainly have oblate to ellipsoidal ascospores with a furrow or slit. The conidia are mostly formed on flask shaped or cylindrical phialides. The Trichocomaceae are defined by having asci borne within a tuft or layer of loose hyphae, and ascospores are lacking slits or furrows. The phialides of species belonging to this family are mostly lanceolate or cylindrical. Apinis (1967) introduced Thermoascaceae and noted that the common essential character of genera of this family is the production of firm, somewhat sclerotioid, pseudoparenchymatous cleistothecia. The inclusion of Byssochlamys in this family does not fit in that description because it produces almost naked ascomata. Based on the relative branch length in Fig. 1, another possibility would be to delimit the Thermoascus clade (clade 8) and the Byssochlamys/Paecilomyces clade (clade 9) as separate families. However, there are characters shared by Thermoascus and Byssochlamys including the production of asci in croziers and the formation of smooth or finely roughened ascospores lacking a furrow or slit. The relationship between these two genera is also illustrated by Byssochlamys verrucosa and Thermoascus crustaceus. Byssochlamys verrucosa phenotypically belongs to Byssochlamys, but is positioned phylogenetically in Thermoascus (Fig. 1) and Therm. crustaceus shares a Paecilomyces anamorph with members of the Byssochlamys/Paecilomyces clade. In addition, most members of both genera are thermotolerant or thermophilic.
Table 4
Overview of the classifications of the Trichocomaceae and Eurotiaceae by Benny & Kimbrough (1980), Malloch (1985b), von Arx (1987) and the current study.
| Benny & Kimbrough (1980) | von Arx (1987) | Malloch (1985b) | Current study |
|---|---|---|---|
| Trichocomaceae: | Eurotiaceae: | Trichomoideae: | Aspergillaceae: |
| Aphanoascus | Chaetosartorya | Byssochlamys | Aspergillus (incl. teleomorphs, syn. Stilbothamnium) |
| Byssochlamys | Cristaspora | Dendrosphaera | Hamigera (incl. Merimbla) |
| Chaetosartorya | Dichlaena | Sagenoma | Leiothecium |
| Dichotomomyces | Talaromyces | Monascus (incl. Basipetospora) | |
| Dichleana | Emericella | Trichocoma | Penicilliopsis |
| Edyuillia | Eupenicillium | Dichlaenoideae: | Penicillium (syn. Chromocleista, Eladia, Eupenicillium, Hemicarpenteles, Thysanophora, Torulomyces) |
| Emericella | Eurotium | Chaetosartorya | Phialomyces |
| Eupenicillium | Fennellia | Cristaspora | Phialosimplex |
| Eurotium | Hemicarpenteles | Dichlaena | Polypaecilum |
| Fennellia | Mallochia2 | Dichotomomyces | Sclerocleista |
| Hamigera | Neosartorya | Eupenicillium | Warcupiella (incl. Raperia) |
| Hemicarpenteles | Saitoa | Edyuillia (=Eurotium) | Xeromyces |
| Hemisartorya | Emericella | Thermoascaceae: | |
| Neosartorya | Eurotium | Paecilomyces (incl. Byssochlamys) | |
| Penicilliopsis | Fennellia | Thermoascus (syn. Coonemeria, Dactylomyces) | |
| Petromyces | Hamigera | Trichocomaceae: | |
| Roumegueriella1 | Hemicarpenteles | Dendrosphaera (tentatively, fide Malloch 1985b) | |
| Sagenoma | Hemisartorya3 | Rasamsonia | |
| Sclerocleista | Neosartorya | Sagenomella | |
| Talaromyces | Penicilliopsis | Talaromyces (syn. Sagenoma, Erythrogymnotheca) | |
| Trichocoma | Petromyces | Thermomyces | |
| Warcupiella | Sclerocleista | Trichocoma | |
| Monascaceae: | Thermoascus | Unknown status: | |
| Ascorhiza | Warcupiella | Ascorhiza (no strains available/studied) | |
| Leiothecium | Pseudocordyceps | ||
| Monascus | Sarophorum | ||
| Xeromyces | Dichleana |
The genera Chaetosartorya, Cristaspora, Dichlaena, Dichotomomyces, Eupenicillium, Edyuillia, Emericella, Eurotium, Hamigera, Hemicarpenteles, Hemisartorya, Neosartorya, Penicilliopsis, Petromyces, Sclerocleista, Thermoascus and Warcupiella were placed by Malloch (1985a, b) in Aspergillaceae (as subfamily Dichlaenoideae). The majority of these genera are also included in our classification, and exceptions are Edyuilla, which is synonymised with Eurotium (von Arx 1974) and Thermoascus, which is classified in Thermoascaceae. The main difference is the placement of Monascaceae is Aspergillaceae. Benny & Kimbrough (1980) placed the genera Ascorhiza, Leiothecium, Monascus and Xeromyces in Monascaceae and suggested a relationship with Ascosphaerales. Later, several authors included this family in Pezizales (Malloch 1981, Hawksworth & Pitt 1983). Von Arx (1987), in his revision of Eurotiales, included Monascus in Onygenaceae, and reduced Monascaceae to synonymy. More recently, Monascaceae was placed in Eurotiales (LoBuglio et al. 1993, Hawksworth et al. 1995). Fennell (1973) noted that species of both Monascaceae and Eurotiaceae, which approximates our definition Aspergillaceae, form a distinct cleistothecial wall. Nevertheless, Fennell (1973) separated these families based on the formation of aleurioconidia by members of Monascaceae, but our results show that this feature is insufficient for family delimitation. Anamorph genera were not treated by Malloch (1985a, b) and Fig. 1 shows that the genera Aspergillus, Basipetospora, Eladia, Fraseriella, Penicillium, Phialomyces, Phialosimplex, Polypaecilum, Thysanophora and Torulomyces are classified in Aspergillaceae. The teleomorph genera Chromocleista, Fennellia, Neocarpenteles and Neopetromyces, which were not treated in Malloch's study (1985a, b), also belong to this family.
The genera Byssochlamys, Dendrosphaera, Sagenoma, Talaromyces and Trichocoma were placed by Malloch (1985a, b) in Trichocomaceae (as subfamily Trichomoideae), and anamorphs in Paecilomyces or Penicillium were linked to it. The results of our phylogenetic analysis (Fig. 1) confirm the positioning of the genera Sagenoma, Talaromyces and Trichocoma in this family. In addition, the recently described genus Rasamsonia (Houbraken et al. 2011d), and the asexual genera Thermomyces andSagenomella are classified in this family. Phylogenetic analysis shows that Byssochlamys is more closely related to Thermoascus. Fennell (1973) also observed the relationship between these two genera and stated that Byssochlamys is transitional between Thermoascaceae and Aspergillaceae (as Eurotiaceae). No strains of the genus Dendrosphaera were available and its position remains questionable. Kobayasi (1971) described an aleurioconidial state in Dendrosphaera eberhardtii and Benny & Kimbrough (1980) therefore suggested placing this species in Onygenales (which makes Dendrosphaeraceae a family of Onygenales). On the other hand, Malloch (1985b) noted that D. eberhardtii and T. paradoxaproduce similar brushes of soft hyphae bearing asci and ascospores suggesting the placement in Trichocomaceae. Following Malloch (1985b), we tentatively place this genus in Trichocomaceae, and consequently, Dendrosphaeraceae are synonymised with Trichocomaceae.
Phylogeny of Aspergillaceae
Seven clades (Fig. 1, clades 1–7) can be distinguished in Aspergillaceae. Each clade is discussed and phenotypic characters of the members belonging to those clades are compared with those of Penicillium.
Clade 1: Penicillium sensu stricto
Penicillium sensu lato is polyphyletic and species of this genus occur in the phylogenetically redefined families Aspergillaceae and Trichocomaceae (Fig. 1). The type species of Penicillium, Penicillium expansum, and the type species of Eupenicillium, E. crustaceum, form a clade within Aspergillaceae, defined here as Penicillium sensu stricto. The Penicillia not belonging to Penicillium s. str. are mainly classified in Trichocomaceae, in a clade together with the type species of Talaromyces, T. flavus (clade 10). The presence of two major clades in Penicillium is concordant with earlier studies using rDNA sequences (Berbee & Taylor 1995, Ogawa et al. 1997, Sugiyama 1998, Ogawa & Sugiyama 2000, Tamura et al. 2000). More recently, Wang & Zhuang (2007) used partial calmodulin sequences for the phylogenetic analysis of Penicillium and their data also supported the presence of two lineages in Trichocomaceae. However, their placement of Talaromyces trachyspermus on a single lineage is contradictory with our data. The Penicillium s. str. clade is most closely related to the Aspergillus clade (clade 2) and is phylogenetically more distant from genera with similar anamorphs such as Paecilomyces, Merimbla and the Penicillium species assigned to Trichocomaceae in this study. The phylogenetic study shows that various other genera belong to Penicillium s. str. The type species of the genera Chromocleista, Torulomyces, Thysanophora, Hemicarpenteles and Eladia are positioned in Penicillium s. str. These genera are considered here as synonyms of Penicillium, and the species are transferred as appropriate. Two well-supported subclades (Fig. 1A, B) can be distinguished within Penicillium s. str. Pitt (1980) classified Penicillium in four subgenera: Aspergilloides, Furcatum, Penicillium and Biverticillium. This system was mainly based on conidiophore branching and shape of the phialides. The type species of subgenus Penicillium (P. expansum) belongs to clade 1B and mainly comprises the species which are ter- and/or quarterverticillate. The type species of the subgenera Aspergilloides and Furcatum (P. aurantiobrunneum (= P. glabrum) and P. citrinum, respectively) are positioned in clade 1A, and monoverticillate and biverticillate species with flask shaped phialides more frequently occur in this clade. The type species of subgenus Biverticillium, Penicillium minioluteum, does not belong to Penicillium s. str. and is recombined as Talaromyces minioluteus elsewhere (Samson et al. 2011). Species with symmetrical biverticillate conidiophores and lanceolate phialdes belong to this clade. These observations confirm other studies that also showed that the current phenotype-based subgeneric classification, which is mainly based on the branching system of the Penicillium conidiophores, is incongruent with the molecular phylogeny (Peterson 2000a, Wang & Zhuang 2007). It is proposed here to abandon the current subgeneric classification and to synonymise subgenus Furcatum with Aspergilloides, because the latter is an older name. The subgenera Aspergilloides and Penicillium correspond to clades 1A and 1B, respectively. The phylogenetic structure within these clades is examined with more depth in Part 3 of the discussion.
Clade 2: Aspergillus
A limited number of Aspergillus species and related teleomorphs are included in this study. The majority of the studied Aspergillus strains form a clade with 51 % bootstrap and 1.00 posterior probability support and this clade is defined here as Aspergillus sensu stricto. Aspergillus s. str. is phylogenetically closely related to Penicillium s. str. (77 % bs, 1.00 pp). These genera are morphologically distinct. Aspergillus forms nonseptate stipes, which often terminate in a distinct inflated part (vesicle) and have a foot-cell (Raper & Fennell 1965). Furthermore, the phialides are produced synchronously from the vesicle in Aspergillus. The distinction between these two genera is largely supported by the phylogeny. However, there are a few exceptions. Aspergillus paradoxus, A. crystallinus and A. malodoratus phylogenetically belong to Penicillium (R.A. Samson, unpubl. data). However, Raper & Fennell (1965) also noted that A. crystallinus and A. malodoratus produce triseriate structures that resemble Penicillium. In addition, there are also Aspergilli, which look similar to Penicillium. An example is Penicillium inflatum, which phylogenetically belongs to Aspergillus section Cremei and will be transferred from Penicillium to Aspergillus (R.A. Samson, unpubl. data). In addition, Aspergillus sydowii regularly produces small penicilli, and A. restrictus can produce diminutive vesiculate monoverticillate stipes, similar in appearance to those of some Penicillium species.
The classification of the genus Aspergillus is traditionally based on morphological characters. Raper & Fennell (1965) divided the genus into 18 groups. More recently, Peterson (2008) studied the relationship among Aspergilli using a multigene phylogeny and accepted 5 subgenera (Aspergillus, Circumdati, Fumigati, Nidulantes and Ornati) and 16 sections. Our data largely corresponds with Peterson's phylogeny, and four of the six subclades in Fig. 1 represent the Aspergillus subgenera as defined by Peterson (2008). However, there are some discrepancies. Sections Restricti and Aspergillus of the subgenus Aspergillus are on a well supported branch (100 % bs, 1.00 pp), confirming Peterson's data. Peterson (2008) placed sections Clavati and Fumigati in a single subgenus and, because of lack of statistical support, tentatively placed section Cervini in this subgenus. The representatives of section Cervini (Aspergillus cervinus, A. kanagawaensis) used in our study show that this section is basal to sections Fumigati and Clavati and belongs in the subgenus Fumigati. This confirms the phenotypic data of Gams et al. (1985), who placed sections Fumigati and Cervini in subgenus Fumigati. Phylogenetically, the monophyletic subgenus Circumdati as proposed by Peterson (2008) contains sections Circumdati, Candidi, Flavi, Flavipedes, Nigri, Terrei and Cremei. The relationship between the former six sections is poorly supported in our analysis (30 % bs, 0.94 pp) and more studies on the phylogenetic structure of Aspergillus are needed. In contrast to previous published results (Peterson 1995, 2008), section Cremei appeared to be unrelated to the other sections of subgenus Circumdati. The studied members of section Cremei (A. pulvinus, A. wentii, A. brunneouniseriatus) formed a well supported clade with the type species of Cristaspora (C. arxii) and this clade is more closely related to members of the subgenus Aspergillus (64 % bs, 1.00 pp) than to subgenus Circumdati. The subgenus Nidulantes contains sections Nidulantes, Ochraceorosei, Usti, Sparsi and Aeni (Frisvad et al. 2005, Peterson 2008, Varga et al. 2010). These results were confirmed in our study, with exception of section Aeni, because no representatives were included in our study. Section Ornati in subgenus Ornati is not positioned in Aspergillus s. str. and species belonging to this section are placed in the clade 7. Peterson (2008) suggested that it would be possible to change the classification of Aspergillus by splitting the genus based on teleomorphic states associated with particular monophyletic groups. However, he advocated keeping Aspergillus as a monophyletic genus, since this would reflect the actual relationships of species displaying an aspergillum whereas dividing the form genus into several genera based on teleomorphs would de-emphasise the relationships for most biologists not intimately familiar with the genus. Teleomorph genera associated with Aspergillus anamorphs include Chaetosartorya, Dichotomomyces, Emericella, Eurotium, Fennellia, Neocarpenteles, Neopetromyces, Neosartorya and Petromyces.
The type species of the genera Polypaecilum and Phialosimplex and the ex-type strain of Basipetospora halophilica form a strongly supported clade (100 % bs, 1.00 pp) within Aspergillus s. str. This clade is related to Aspergillus sections Cremei, Aspergillus and Restricti (64 % bs, 1.00 pp). Recently, Phialosimplex was introduced for species with simple phialides borne laterally on vegetative hyphae. These phialides form chains of conidia and are mostly monophialidic, but a second opening can also be formed (polyphialides). Sagenomella chlamydosporus and S. sclerotialis were transferred to this genus and Phialosimplex canicus was described as a new species (Sigler et al. 2010). The transfer of S. sclerotialis to Phialosimplex created a paraphyletic genus with Polypaecilum embedded in it. The type species of Polypaecilum, P. insolitum, produces its conidia on polyphialides and this feature is shared with members of Phialosimplex (Smith 1961a). The formation of chlamydospores and the occurrence in patient material are also shared features of both genera. This indicates that these genera could be congeneric and more research is needed to clarify their taxonomic status. Basipetospora halophilica also belongs to this diverse clade. The production of short solitary conidiophores or conidiogeneous cells by this species is a shared character with members of Phialosimplex, Polypaecilum and many other genera; however, formation of polyphialides by this species was not described (Pitt & Hocking 1985). Furthermore, Polypaecilum morphs related to Thermoascus and Dichotomyces are not part of this clade and this genus is polyphyletic.
Clade 3: Hamigera
Hamigera, Warcupiella and the related anamorphs Merimbla and Raperia are positioned in clade 3. The statistical support of this clade is low (< 70 % bs, < 0.90 pp) and the studied species might not be related. We decided to place the species Hamigera avellanea, Hamigera striata, Penicillium megasporum, Talaromyces leycettanus and Warcupiella spinosa in our taxon sampling based on data presented in previous studies, in which it was demonstrated that these species are related (Ogawa & Sugiyama 2000, Tamura et al. 2000, Peterson 2008, Peterson et al. 2010). Penicillium giganteum, Merimbla ingelheimensis, Hamigera paravellanea, H. insecticola, H. inflata, H. terricola, H. pallida, H. fusca were not included in our study, but are also members of this clade (Ogawa & Sugiyama 2000, Peterson et al. 2010). Hamigera striata and Talaromyces leycettanus are on a strongly supported branch (94 % bs, 1.00 pp). Ogawa & Sugiyama (2000) showed in their 18S rDNA analysis that both species are related (83 % bs), confirming our data. Peterson et al. (2010) did not accept H. striata in Hamigera because of lack of statistical support and followed Benjamin's (1955) placement of this species in Talaromyces. Our results indicate that Talaromyces is phylogenetically distant and we therefore maintain H. striata in Hamigera. Talaromyces leycettanus also warrants further attention. Stolk & Samson (1972) noted that the anamorph of T. leycettanus, Paecilomyces leycettanus, seems to occupy an intermediate form between Penicillium and Paecilomyces. The complex conidiophore of T. leycettanus resembles Merimbla (= anamorph of Hamigera) (Peterson et al. 2010), supporting its placement in this diverse clade. Warcupiella is monotypic, represented by Warcupiella spinulosa (Subramanian 1972) and this species was originally described as Aspergillus spinulosus (Raper & Fennell 1965). Later, Raperia was introduced by Subramanian & Rajendran (1979) to accommodate the anamorph of W. spinulosa (von Arx 1986). Our results and others (Tamura et al. 2000, Peterson 2008) show that W. spinulosa does not belong to Penicillium or Aspergillus, and is more closely related to Hamigera avellanea. The relationship between Warcupiella/Raperia and Hamigera was also noted by von Arx (1986), and he transferred W. spinulosa to Hamigera. Penicillium megasporum, another member of this clade, has little affinity with Penicillium s. str. as noted by Pitt (1980), who created Penicillium series Megaspora for this species and P. asperosporum. Peterson et al. (2010) described the penicillus structure of P. megasporum as similar as that of Merimbla, but that phylogenetic analysis did not support inclusion of P. megasporum in the Hamigera clade. Our analysis lacks high bootstrap support to confidentially place P. megasporum, W. spinulosa and T. leycettanus in Hamigera. More research is needed to elucidate the classification of this diverse clade.
Clade 4: Penicilliopsis
Clade 4 comprises Aspergillus zonatus and Penicilliopsis clavariiformis and these two species form a strongly supported clade. Penicilliopsis is typified by P. clavariiformis and characterised by seed-borne, stipitate stromata. The anamorph genera Pseudocordyceps, Sarophorum and Stilbodendron are phenotypically related (Samson & Seifert 1985, Hsieh & Ju 2002). The former two genera have conidiogenous structures similar to those of Penicillium and the latter has Aspergillus-like conidiogenous structures. The sclerotia of Stilbothamnium morphologically resemble ascomata of Penicilliopsis. However, phylogenetically, the type species of Stilbothamnium, Aspergillus togoensis, belongs to Aspergillus subgenus Circumdati section Flavi and is unrelated to Penicilliopsis (Fig. 1). More research is needed to clarify the relationship between Penicillium, Penicilliopsis and the associated anamorph genera Pseudocordyceps and Sarophorum.
Clade 5: Monascus, Xeromyces and Leiothecium
The teleomorph genera Monascus, Xeromyces and Leiothecium belong in clade 5, as do the anamorph genera Fraseriella and Basipetospora (Pettersson et al. 2011, our data). Benny & Kimbrough (1980) placed Monascus, Xeromyces and Leiothecium in Monascaceae and this family is transferred here to Aspergillaceae (see part 1, phylogeny of Aspergillaceae). These genera have similar phenotypic characters including the formation of stalked ascomata and the production of aleurioconidia from undifferentiated conidiogenous cells. These features clearly set these genera apart from Penicillium s. str. and Aspergillus. Our results confirm those of Pettersson et al. (2011) and we follow their opinion in retaining Xeromyces for xerophilic Monascus-like species and Monascus for the species that grow at higher water activities. In addition, Pettersson et al. (2011) suggested that Chrysosporium inops should be transferred to a new genus. However, Fig. 1 shows that this species is closely related to X. bisporus and the xerophilic nature of boths species indicates a close relationship (Pitt & Hocking 2009, Pettersson et al. 2011). Leiothecium is basal to Monascus and the connection between these two genera was also noted by Samson & Mouchacca (1975). Aspergillus clavatoflavus is basal to this clade, but the relationship lacks statistical support. The micromorphology is A. clavatoflavus differs from the members of clade 5 and therefore this species is placed outside this clade, awaiting more conclusive data.
Clade 6: Phialomyces
The type species of Phialomyces, Phial. macrosporus (Misra & Talbot 1968), is positioned in clade 6 and is closely related to Penicillium arenicola (100 % bs, 1.00 pp). Merimbla humicoloides (= Penicillium humicoloides sensu Peterson et al. 2010) also belongs to this clade (R.A. Samson, unpubl. data). All three species are phylogenetically distinct form Penicillium s. str. Pitt (1980) placed P. arenicola in a separate section and series and noted that this species may not be a true Penicillium. Phenotypically, Phial. macrosporus, M. humicoloides and P. arenicola form conidia in shades of gold-brown, a feature uncommon for Penicillium species. These species can produce terverticillate conidiophores, a character also present in subgenus Penicillium (clade 1B). Our results indicate that P. arenicola and M. humicoloides should be transferred to another genus.
Clade 7: Sclerocleista
Sclerocleista ornata and S. thaxteri are basal to Phial. macrosporus and P. arenicola (Fig. 1). Sclerocleista ornata was originally described as Aspergillus ornatus (Raper et al. 1953), and later transferred to Sclerocleista (Subramanian 1972). Sclerocleista thaxteri was originally described in Sclerocleista and later von Arx (1974) transferred this species to Hemicarpenteles. The two species are closely related, and phylogenetically distant from H. paradoxus, the type species of Hemicarpenteles (Fig. 1, Penicillium s. str.). Peterson (2008) placed Sclerocleista basal to the Aspergilli, suggesting a monophyletic Aspergillus clade; however, our data do not support this conclusion. Sclerocleista differs from Penicillium s. str. in having an Aspergillus-type anamorph and purple coloured cleistothecia filled with lenticular ascospores (Raper & Fennell 1965).
Phylogeny of Thermoascaceae
Figure 1 shows that two clades (clade 8 and 9) are present in Thermoascaceae (= lineage 2). The phylogeny of these two clades and the comparison of the species belonging to these two clades with Penicillium s. str. is discussed below.
Clade 8: Thermoascus
Thermoascus aurantiacus, T. crustaceus and T. thermophilus are together with Byssochlamys verrucosa in a separate clade. The taxonomy of Thermoascus is treated in various studies. Apinis (1967) split Thermoascus in two: Thermoascus was retained for its type species T. aurantiacus, and T. thermophilus and T. crustaceus were transferred to Dactylomyces. Later, Mouchacca (1997) divided Dactylomyces further in two, creating Coonemeria for T. crustaceus. Although these species have different anamorphs (Paecilomyces/Polypaecilum), our phylogenetic study (Fig. 1) shows that these three species are closely related and should be retained in Thermoascus. Samson et al. (2009) noted that Byssochlamys verrucosa is misidentified in Byssochlamys but related to Thermoascus, and this observation is confirmed here. Thermoascus has a similar type of sclerotioid cleistothecium as members of Penicillium s. str. (Stolk & Samson 1983). These two genera differ mainly in ascomatal development. Ascomata of Thermoascus are initiated by an ascogonial coil (Stolk 1965, Subramanian & Rajendran 1980), whereas in Penicillium s. str. the formation begins with sclerotium-like bodies inside which the ascogonia develop. Furthermore, the anamorphs of Thermoascus are not of the Penicillium type, but can be similar to Paecilomyces.
Clade 9: Paecilomyces
The types of Paecilomyces (P. variotii) and Byssochlamys (B. nivea) occur together on a branch with 100 % bootstrap support. Using a polyphasic approach, Samson et al. (2009) showed that the genera Byssochlamys and Paecilomyces s. str. are closely related and form a monophyletic group. Paecilomyces was introduced by Bainier (1907) and has priority over Byssochlamys (Westling 1909). Phylogenetic analysis of the 18S rDNA demonstrated that Paecilomyces sensu Samson (1974) is polyphyletic across two subclasses, Sordariomycetidae and Eurotiomycetidae. The type species of this genus, Paecilomyces variotii, and its thermophilic relatives belong in the Eurotiales (Luangsa-ard et al. 2004). Figure 1 shows that Paecilomyces s. str. is also phylogenetically distinct from Penicillium. Morphological characters also support this conclusion. The conidia of Paecilomyces s. str. are olive-brown and formed in phialides that have a broad base and end in a long and slender neck, while the conidia of Penicillium species are green and formed in flask or cylindrical shaped phialides. In addition, the conidiophores of Paecilomyces s. str. are more irregularly branched than those of Penicillium. The teleomorphs are also different: those of Paecilomyces (formerly known as Byssochlamys) are almost naked while Penicillium s. str. produces cleistothecia with a distinct wall.
Phylogeny of Trichocomaceae
Five clades (clades 10–15) can be recognised in the more narrowly delimited Trichocomaceae. The species treated in these clades are phylogenetically distinct from Penicillium s. str., but some are phenotypically similar.
Clade 10: Talaromyces
The majority of Penicillium species assigned to the subgenus Biverticillium belong in clade 10 (incl. type of subgenus Biverticillium, P. minioluteum) together with the type species of the genera Talaromyces and Sagenoma. These species are phylogenetically distant from Penicillium s. str. and therefore these species are transferred to the genus Talaromyces (Samson et al. 2011, this study). Phenotypically, Talaromyces differs from Penicillium s. str. by the formation of symmetrically branched conidiophores with lanceolate phialides, and the production of soft ascomata without a well-defined, persistant wall. Members of the Talaromyces clade grow slower on the agar medium G25N than Penicillium s. str. members (Pitt 1980). Also differences in ubiquinones and extrolites patterns are observed between Penicillium sensu stricto and Talaromyces. The Q9 ubiquinone system was present in most Penicillium sensu stricto species, while nearly all Talaromyces have Q10(H2) (Paterson 1998). In addition, extrolites such as mitorubrins, certain bisanthraquinones (rugulosin, skyrin), duclauxin and glauconic acide were detected in Talaromyces, but never found in Penicillium sensu stricto (Frisvad et al. 1998). The taxonomic and phylogenetic structure of Talaromyces is considered further by Samson et al. (2011).
The neotype strain of Aphanoascus cinnabarinus sensu Udagawa and Takada also belongs to this clade. Much taxonomic confusion followed after the proposal of Aphanoascus by Zukal (1890). Most authors follow Apinis (1968) and maintain Aphanoascus that is typified by A. fulvescens. In addition, the neotypification of A. cinnabarinus by Udagawa & Takada (1973) was incorrect, because their neotype strain had a Paecilomyces anamorph, while Zukal's original description and illustrations showed structures of a Chrysosporium anamorph (Stolk & Samson 1983). Based on morphological characters, Stolk & Samson (1983) suggested that Chromocleista cinnabarina (as A. cinnabarinus sensu Udagawa & Takada) belongs to Eurotiales, and that this species occupies an intermediate position between the genera Thermoascus and Talaromyces. The result of our multigene phylogeny shows that C. cinnabarina belongs to Talaromyces s. str.
This data is in concordance with the 18S rDNA sequence data of Ogawa & Sugiyama (2000), which shows that C. cinnabarina forms a monophyletic group with T. macrosporus and T. bacillisporus. No specimens of Erythrogymnotheca were studied, but an ITS sequence of the type species of this genus (E. paucispora) is deposited GenBank (AB176603) and a BLAST search on GenBank and internal CBS databases shows that this sequence belongs to Talaromyces s. str.
Clade 11: Thermomyces
Talaromyces thermophilus belongs to the same clade as the type of Thermomyces, T. lanuginosus. Talaromyces thermophilus and Therm. lanuginosus share similar characters, including their ability to grow at high temperatures and the formation of thick-walled chlamydospores or chlamydospore-like conidia. These characters are not shared by members of Penicillium s. str. Talaromyces luteus is basal to this clade. This species is not thermophilic and phenotypically different from Thermomyces and Tal. thermophilus, and it is therefore excluded from clade 11.
Clade 12: Sagenomella
Clade 12 is centered around the type species of Sagenomella, S. diversispora, and this genus is phylogenetically unrelated to Penicillium s. str. Sagenomella was described by Gams (1978) for Acremonium-like fungi and is characterised by connected conidial chains and sympodially proliferating, often centrally swollen phialides. These characters are not present in Penicillium s. str. Molecular data showed that Sagenomella sensu Gams is polyphyletic (Endo et al. 1998, Thanh et al. 1998, our results). Sigler et al. (2010) transferred S. chlamydospora and S. sclerotialis to the new genus Phialosimplex and Sagenomella bohemica belongs in Talaromyces (Samson et al. 2011). The close relationship of this genus with Talaromyces indicates that Sagenomella is a reduced form of Talaromyces.
Clade 13: Rasamsonia
The thermophiles Talaromyces emersonii and T. byssochlamydoides were transferred to Rasamsonia (Houbraken et al. 2011d), leaving T. thermophilus as sole thermophile in Talaromyces. However, our phylogenetic analysis shows that this species belongs to Thermomyces and not to Talaromyces. The genus Rasamsonia was erected for thermotolerant or thermophilic species, which have cylindrical phialides usually gradually tapering towards the apices, conidiophores with distinctly rough walled stipes, olive-brown conidia and ascomata, if present, with a scanty covering. This clade contains the species R. argillacea, R. brevistipitata, R. byssochlamydoides, R. cylindrospora, R. eburnea and R. emersonii (Houbraken et al. 2011d).
Clade 14: Trichocoma
The monotypic genus Trichocoma is typified by Trichocoma paradoxa and is characterised by asci born in hyphal masses or tufts that can be up to 10–20 mm long (Kominami et al. 1952, Malloch 1985b). The anamorph of this species resembles an anamorph of Talaromyces. However, Trichocoma produces conidia in shades of brown. Rasamsonia is phylogenetically related to Trichocoma, and can be differentiated by the presence of scanty ascomatal coverings and its ability to grow at temperatures above 40 °C.
Excluded genera: Geosmithia, Phialotubus and Yunnania
The genera Geosmithia, Phialotubus and Yunnania have sometimes been hypothesised to be related to Penicillium (Gams 1978, Pitt 1980, Kong 1998). Our data shows that these genera do not belong to the Eurotiales and details are provided below.
Geosmithia
The genus Geosmithia is typified by G. lavendula (Pitt 1978) and is a polyphyletic morphogenus introduced to classify Penicillium species, which are characterised by: a) cylindroidal phialides and conidia, b) rugulose to rugose conidiophores walls, metulae and phialides and c) conidial colour other than green (with the exception of G. namyslowskii). Anamorphs of Geosmithia have affinities with hypocrealean (Hypocreales: Bionectriaceae) and eurotialean (Eurotiales: Trichocomaceae) fungi, and the type species of Geosmithia, G. lavendula, is related to Acremonium alternatum, the type species of Acremonium (Ogawa et al. 1997, Rossman et al. 2001, Summerbell et al. 2011). Currently, there are 16 described species (Pitt 1980, Yaguchi et al. 1993, 1994, Pitt et al. 2000, Kolařík et al. 2004, 2005, 2010), and eight of these species (G. fassatiae, G. flava, G. langdonii, G. lavendula, G. morbida, G. obscura, G. pallida, and G. putterillii) belong to the Hypocreales. Geosmithia argillacea (teleomorph Talaromyces eburneus sensu Yaguchi et al. 2005), G. eburnea (teleomorph Talaromyces eburneus sensu Yaguchi et al. 1994), G. emersonii (teleomorph Talaromyces emersonii) and G. cylindrospora are closely related to each other and were recently transferred to Rasamsonia (Houbraken et al. 2011d, see clade 13 above). Geosmithia swiftii (teleomorph Talaromyces bacillisporus) and G. viridis belong to Talaromyces s. str. and G. namyslowskii and G. malachiteum (described as the anamorph of Chromocleista malachitea) belong to Penicillium s. str. (Fig. 1). Zaleski (1927) originally described Geosmithia namyslowskii as Penicillium namyslowskii and the new combination of Penicillium malachiteum is made elsewhere in this article.
Phialotubus
Phialotubus (Roy & Leelavathy 1966) is monotypic with Phialotubus microsporus as the type. This species is characterised by the formation of cylindrical phialides with long hyaline thread-like projections, which get prolonged into the hyaline tube-like projection when conidia are formed (Fig. 2). The conidia are fusiform in shape and produced in chains (Roy & Leelavathy 1966, Gams 1978, Arx 1981). These characters suggest a close connection with the Eurotiales, for example with Paecilomyces, Phialomyces,Sagenomella and Torulomyces. However, a BLAST search on GenBank with an ITS sequence of strain CBS 861.70isoT (GenBank no. JN831360) did not retrieve any high similarity matches with members of the Eurotiales. The overall similarity matches were low and this species probably belongs to the class Sordariomycetes.
Phialotubus microsporus CBS 861.70isoT. A. Colonies grown for 7 d at 25 °C, from left to right: CYA, MEA, OA. B–D. Conidiophores and conidia. Scale bar = 10 μm.
Yunnania
Kong (1998) proposed the genus Yunnania and typified it with Y. penicillata. The truncated conidia and the black or brownish black colonies resemble those of Scopulariopsis. In addition, the conidia are produced by annelides (Fig. 3). Examination of the type strain of Y. penicillata (CBS 130296T) showed that this species is morphologically related to Scedosporium. A BLAST search on GenBank with an ITS sequence of this species (GenBank no. JN831361) did not retrieve a high similarity match, but showed that this species belongs to the order Microascales.
Yunnania penicillata CBS 130296T. A. Colonies grown for 7 d at 25 °C, from left to right: MEA, OA, CYA. B–D. Conidiophores and conidia.
Taxonomic implications
Aspergillaceae Link, Abh. dt. Akad. Wiss. Berlin 1824: 165. 1826.
= Eurotiaceae Clements and Shear, Gen. Fung. 50. 1931.
= Monascaceae J. Schröter, Nat. Pflanzenfamilien 1: 148. 1894.
= Hemicarpenteleaceae Locquin, Tribune Méd. (Paris) 1. 1972. nom. inval. (Art. 36).
= Penicilliaceae Vuillemin, Pl. Jungh. 10: 172. 1910. (as Penicilliacées nom. inval. Art. 32.1b).
= Penicilliopsidaceae Locquin, Tribune Méd. (Paris) 1. 1972. nom. inval. (Art. 36).
= Phialomycetaeae Locquin, Mycologie générale et structurale: 212. 1984. nom. inval. (Art. 36).
= Warcupiellaceae Locquin, Mycologie générale et structurale: 167. 1984. nom. inval. (Art. 36).
= Xeromycetaceae Locquin, Tribune Méd. (Paris) 1. 1972. nom. inval. (Art. 36).
Type: Aspergillus Fr: Fr.
Thermoascaceae Apinis, Trans. Br. Mycol. Soc 50: 581. 1967.
Type: Thermoascus Miehe
Trichocomaceae E. Fischer, Nat. Pflanzenfam. 1: 310. 1897. (as Trichocomataceae)
= Talaromycetaceae Locquin, Mycologie générale et structurale: 176. 1984. nom. inval. (Art. 36).
= Dendrosphaeraceae Ciferri ex Benny & Kimbrough, Mycotaxon 12: 22. 1980.
Type: Trichocoma Junghuhn
Part Two: delimitation of Penicillium
Authority
The generic name Penicillium is attributed to Link (1809). Link included three species within Penicillium, P. glaucum, P. candidum and P. expansum. He illustrated P. candidum, which clearly shows structures of a Penicillium species. Later, Penicillium expansum was selected by Thom (1910) and later (co-)authors as the lectotype of Penicillium. The generic name Penicillium was attributed by Fries (1832: 406) to Link (1809). Hawksworth et al. (1976) proposed to conserve the generic name Penicillium as Penicillium Link ex Grey over Penicillium Fries 1832 (proposal no. 420), and lectotypified the genus with Penicillium expansum Link ex Grey. This proposal was countered by Jørgensen & Gunnerbeck (1977) because Fries listed “Mucor crustaceus L.” as a typical species of Penicillium and not as the type species of this genus. The proposal of Hawksworth et al. (1976) was therefore rejected (Petersen 1980). The general starting point for fungal names is Linnaeus 1753, but there are a few exceptions and these are mentioned in the ICBN under art. 13e. One exception is that names used by E.M. Fries' “Systema mycologicum” 1821–1832 have a protected status. These names are sanctioned and have priority over older synonyms and homonyms. The authority used here is therefore Penicillium Link: Fries.
Generic diagnosis
The concept of Penicillium has been refined and restated often in mycological history. The concept of Raper & Thom (1949) is followed here; however, there are some emendations. In our concept, Penicillium includes species with pigmented stipes (Thysanophora species, P. stolkiae and related species), as well as species formerly ascribed to the genera Eladia, Torulomyces, Chromocleista and Hemicarpenteles. Details regarding the position of these genera in Penicillium are presented below. Another important difference between our and Raper & Thom's (1949) concept is the exclusion of Talaromyces and related Penicillium species. In our concept, only teleomorphs producing pseudoparenchymatous and sclerotioid ascomata are included (“Eupenicillium-type”), and Talaromyces species, with soft ascomata without a well-defined, persistent wall, are excluded (Samson et al. 2011). Also the Penicillium species, which have lanceolate phialides and metulae with equal lengths as the phialides, are excluded. These species are also phylogenetically distinct (Fig. 1). Our emended generic diagnosis is derived from Raper & Thom (1949) and is presented here:
Penicillium Link: Fries, Systema Mycologicum 3: 406. 1832.
Vegetative mycelium abundant, entirely submerged or more or less effused, irregularly branching, septate, hyaline or brightly coloured and forming a dense and compact mycelia colony with well-defined margins. Conidiophores borne from undifferentiated subsurface, superficial or aerial hyphae, rarely subapically proliferation under terminal penicillus. Stipes relatively narrow and thin walled, 2–5 μm, and in some species apically swollen, hyaline, in some species brown. Conidial apparatus usually a well defined structure (brush or broom), named the Penicillus; penicilli comprised of phialides born directly on the stipe, or with one, two or rarely more verticils of metulae and rami as supporting cells. Conidiogenous cells phialides, borne in succession, i.e. not synchronouse, rarely exceeding 15 μm in length, ampulliform, rarely cylindrical. Conidia in unbranched chains, borne basipetally, single celled, commonly between 2–5 μm in diameter, rarely exceeding 6 μm, en masse coloured in shades of green, rarely white, olive or brown. Chlamydospores absent. Sclerotia occasionally produced, composed of thick-walled cells, usually hard. Cleistothecia, if produced, usually hard, globose to subglobse, pseudoparenchymatous or sclerochymatous, ripening from the center outward and often tardily; white, pale, yellow, orange or brown coloured, occasionally black or red. Asci ellipsoidal to globose, usually 8-spored, 5–15 μm. Ascospores lenticular, usually with equatorial ridges, 2–5 μm.
Synonyms of Penicillium
The re-definition of the genus Penicillium has several taxonomic implications. Based on the phylogenetic data presented in Fig. 1 in combination with a review of literature, we place the genera Chromocleista, Carpenteles, Citromyces, Eladia, Eupenicillium, Hemicarpenteles, Thysanophora and Torulomyces in synonymy with Penicillium. More genera are congeneric with Penicillium and a more extended list can be found in Seifert et al. (2011: 333). Each genus is discussed here and new combinations are proposed below for the species accommodated in these genera.
Penicillium Link: Fries, Systema Mycologicum 3: 406. 1832.
= Penicillium Link, Obs. Mycol 1: 16. 1809 (nom. inval., Art. 13e).
= Coremium Link ex Gray, Nat. Arr. Br. Pl. 1: 563. 1821.
= Eupenicillium Ludwig, Lehrb. Nied. Kryptog.: 263. 1892.
= Citromyces Wehmer, Bleitr. Kennt. Pilze 1: 1. 1893.
= Carpenteles Langeron, C.r. Séanc. Soc. Boil. Paris 87: 344. 1922.
= Torulomyces Delitsch, Systematik der Schimmelpilze: 91. 1943.
= Thysanophora Kendrick, Can. J. Bot. 39: 820. 1961.
= Eladia Smith, Trans. Brit. Mycol. Soc. 44: 47. 1961.
= Hemicarpenteles Sarbhoy & Elphick, Trans. Brit. Mycol. Soc. 51: 156. 1968.
= Penicillium Link ex Gray sensu Pitt, The Genus Penicillium: 154. 1980 (nom. inval., art 13e).
= Chromocleista Yaguchi & Udagawa, Trans. Mycol. Soc. Japan 34: 101. 1993.
Subgenus Aspergilloides Dierckx, Annls. Soc. Scient. Brux. 25: 85. 1901.
= Subgenus Monoverticillium Biourge, Cellule 33: 265. 1923.
= Subgenus Furcatum Pitt, The Genus Penicillium: 233. 1980.
Subgenus Penicillium
= Subgenus Eupenicillium Dierckx, Annls Soc. Scient. Brux. 25: 85. 1901.
Chromocleista
The genus Chromocleista, defined by the type species C. malachitea, belongs to Penicillium and is related to P. herquei (see Figs Figs1,1, ,7).7). This genus was created by Yaguchi et al. (1993) for species that form bright coloured sclerotioid cleistothecia with a Geosmithia anamorph (Fig. 4). The close relationship with Eupenicillium was noted in the original description, but the presence of the Geosmithia anamorph was, according to the authors, sufficient to create a new genus. Using 18S rDNA sequence data, Ogawa & Sugiyama (2000) showed that C. malachitea groups with Eupenicillium javanicum, E. crustaceum, P. chrysogenum and Geo. namyslowskii. Furthermore, they indicated that the Geosmithia-anamorph of Chromocleista malachitea resembles P. herquei and the former species could be placed in synonymy. Comparison of the β-tubulin sequences and RPB2 sequences of the (neo)type cultures of P. herquei CBS 336.48NT and C. malachitea CBS 647.95T showed homologies of 92.8 % and 94.7 % respectively. Furthermore, a BLAST search with the ITS, RPB2 and β-tubulin sequence data of C. malachitea CBS 647.95T on GenBank and local databases did not retrieve any high similarity matches with other described species and therefore this species is combined with Penicillium below.
A–F. Penicillium malachiteum CBS 647.95HT. A. Colonies grown for 7 d at 25 °C, from left to right: MEA, CYA, YES, DG18. B–D. Conidiophores. E. Immature cleistothecia. F. Conidia. G–K. Penicillium sacculum CBS 123567. G. Colonies grown for 7 d at 25 °C, from left to right: MEA, CYA, YES, DG18. H–J. Conidiophores. K. Conidia. Scale bar = 10 μm.
Citromyces
Citromyces was introduced by Wehmer (1893) for monoverticillate Penicillium species. Many authors have agreed that this genus is a synonym of Penicillium (Westling 1911, Biourge 1923, Thom 1930, Raper & Thom 1949, Pitt 1980). Citromyces largely encompasses subgenus Aspergilloides as defined by Pitt (1980). In our classification system, Citromyces corresponds with section Aspergilloides.
Eladia
Thom (1930) and Raper & Thom (1949) regarded Penicillium sacculum Dale as a Scopulariopsis, and Smith (1961b) introduced the genus Eladia to accommodate this species and typified it with E. saccula. Smith (1961b) did not indicate why this species should not be considered a Penicillium. Pitt (1980) accepted the positioning of E. saccula in a separate genus and he noted that this genus is closely related to Penicillium, but differing in three features (Fig. 4): a) the phialides are born irregularly on stipes, b) phialides have a short collula and distinct thickening of the wall; c) the conidial chains are very short. Stolk & Samson (1985) did not accept this genus and transferred E. saccula to Penicillium and this position was retained in the list of accepted species in Trichocomaceae (Pitt et al. 2000). Our molecular data support the positioning of Smith's neotype of Eladia succula (CBS 231.61NT) in Penicillium (Figs (Figs11 and and7).7). This species is most closely related to P. canescens and P. atrovenetum (Fig. 7, clades 24, 25). The relationship of P. sacculum with these species (and also with e.g. P. janczewskii) was also suggested by Stolk & Samson (1985), who emphasised that all these species have swollen phialides with an abruptly narrowed neck and often short conidial chains.
Six species were described in Eladia: E. saccula, E. inflata, E. minima, E. striatispora, E. pachyphialis and E. tibetensis. The current name for Eladia saccula is Penicillium sacculum Dale (1926). Ex-type strains of E. inflata (CBS 127833) and E. minima (CBS 127834) were examined and comparison of the RPB2 region (Fig. 8) showed that E. inflata and P. fuscum (= E. pinetorum, CBS 295.62T) are closely related. Eladia minima is closely related to P. heteromorphum (CBS 226.89T) and P. philippinense (CBS 623.72T). Eladia minima is closely related to P. heteromorphum, P. restrictum, Eup. katangense and Eup. philippinense (data not shown). More research is needed to determine species boundaries in this group of phylogenetical related species. No living ex-type material could be obtained for Eladia striatispora. Drawings of E. striatispora show a clear resemblance with P. striatisporum, and therefore E. striatispora is regarded as a synonym of P. striatisporum (Stolk 1969, Matsushima 1971, Kobayasi 1971). No type material could be obtained from E. pachyphialis and E. tibetensis and their taxonomic position remains uncertain.
Eupenicillium and Carpenteles
The genus Eupenicillium was introduced by Ludwig (1892) for an ascomycete species that Brefeld (1874) described and illustrated as P. crustaceum. Unaware of Ludwig's publication, Langeron (1922) introduced the genus Carpenteles for ascus-producing Penicillium species. Because we include sexual and asexual species in our definition of Penicillium, Eupenicillium and Carpenteles are considered synonyms of Penicillium. In most cases a Penicillium anamorph name is already available for these Eupenicillium species; however, in the case of E. bovifimosum and E. saturniforme, only the teleomorph was described and no Penicillium names linked to these species exist (Tuthill & Frisvad 2002, Wang & Zhuang 2009). The new combinations Penicillium bovifimosum and Penicillium saturniforme are proposed below for these two species.
Hemicarpenteles
The genus Hemicarpenteles was created by Sarbhoy & Elphick (1968) and H. paradoxus was designated as type (IMI 117502T = CBS 793.68T). This species is characterised by the presence of an Aspergillus anamorph and sclerotioid ascomata (Fig. 5). This unique combination led to the proposition of a new genus. If only ascoma development and characteristics were considered, then H. paradoxus is most similar to Eupenicillium, because both genera form sclerotioid cleistothecia that ripen from the centre outwards (Sarbhoy & Elphick 1968, Pitt 1980, Stolk & Samson 1983). Figure 1 shows the phylogenetic positioning of H. paradoxus in the genus Penicillium. The placement of this species in Penicillium is remarkable, since this species has an Aspergillus anamorph. The positioning of H. paradoxus in Penicillium is also supported by analysis of the ITS and D1/D2 regions of the 28S rDNA and partial calmodulin and β-tubulin data (Peterson 2000a, 2008) and the name Penicillium paradoxum will therefore be proposed (R.A. Samson, unpubl. data). The placement of an Aspergillus-type anamorph in the genus Penicillium might be confusing, when using solely phenotypic characters for identification. Three other species are described in Hemicarpenteles: H. acanthosporus, H. ornatus and H. thaxteri. The former species was transferred to Neocarpenteles acanthosporus (Udagawa & Uchiyama 2002) and phylogenetic studies showed that this species is related to Aspergillus section Clavati (Tamura et al. 2000, Varga et al. 2007, Peterson 2000b, 2008). Hemicarpenteles ornatus and H. thaxteri are currently classified in Sclerocleista (Fig. 1, clade 7) (Pitt et al. 2000).
A–G. Penicillium kewense CBS 344.61T. A. Colonies grown for 7 d at 25 °C, from left to right: MEA, CYA, YES, DG18. B–C. Cleistothecia. D-E. Conidiophores. F. Conidia. G. Ascospores. H–N. Aspergillus paradoxus (= P. paradoxum, R.A. Samson unpubl. results) CBS 130295. H. Colonies grown for 7 d at 25 °C, from left to right: MEA (14 d), CYA, YES, DG18. I. Detail of conidiophores. J. Cleistothecia. K–L. Conidiophores. M. Ascospores. N. Conidia. Scale bar = 10 μm.
Thysanophora
Thysanophora was proposed by Kendrick (1961), based on Haplographium penicillioides. Haplographium penicillioides was transferred to Thysanophora because this species produces conidia from phialides in a basipetal succession and in dry chains, while Haplographium species produce ameroconidia in slime. Roumeguère (1890) noted in his description of H. penicillioides that this species also forms Penicillium-like conidiophores (“l'appareil fructifère ressemble à celui d'un Penicillium”). Preuss' description of three new Penicillium species (P. finitimum, P. flexuosum and P. fuscipes) in 1851 from pine needles might be the first report of members Thysanophora. The habitat and descriptions certainly indicate this placement, but unfortunately, no type specimens were maintained (Kendrick 1961).
Thysanophora species produce dark coloured colonies, have dark and stout conidiophores and the majority of species have secondary growth of the stipe by means of the proliferation of an apical penicillius (Fig. 6). Based on the combined RPB1, RPB2, Tsr1 and Cct8 data, it is clear that members of the genus Thysanophora belong to Penicillium. Members of this genus form a separate clade within this genus (Figs (Figs1,1, ,7),7), confirming earlier results using rDNA sequences (Iwamoto et al. 2002, Peterson & Sigler 2002). Although stipe pigmentation of Thysanophora species is brown, this feature is thus not a useful phylogenetic character for separating this genus from Penicillium (Iwamoto et al. 2002). Melanised conidiophores appear in two separated lineages in Penicillium, namely in Thysanophora, and in a second lineage centered on P. stolkiae (Peterson & Sigler 2002). Another characteristic of Thysanophora is the secondary growth of the stipes. This character is not present in any other Penicillium species and could be argued as a feature sufficient to keep Thysanophora as a separate genus. However, that would create a paraphyletic clade in Penicillium or the need for at least eight genera to restore monophyly. To avoid both scenarios it is chosen here to transfer this genus to Penicillium. Thysanophora comprises eight accepted species, namely T. longispora, T. canadensis, T. taxi, T. striatispora, T. asymmetrica, T. verrucosa, T. glaucoalbida and T. taiwanensis (Minter 2007). Thysanophora penicillioides is regarded as a synonym of T. glauco-albida, because following the ICBN, the latter epithet has priority (Morelet 1968, Minter 2007). No type material was present in the CBS culture collection of T. striatispora, T. asymmetrica, T. verrucosa, T. glaucoalbida and T. taiwanensis. Only the species descriptions were studied and the species delimitation of Mercado-Sierra (1998) is largely followed. With exception of T. taxi, which was originally described as Penicillium taxi (Schneider 1956), all accepted species of Thysanophora are transferred here to Penicillium and new combinations are proposed below.
A–H. Penicillium glaucoalbidum CBS 292.60. A. Colonies grown for 7 d at 25 °C, from left to right: MEA, CYA, YES, DG18. B–D. Conidiophores. E. Conidia. F–J. Penicillium lagena CBS 337.97. F. Colonies grown for 7 d at 25 °C, from left to right: MEA, CYA, YES, DG18. G–I. Conidiophores. J. Conidia. Scale bar = 10 μm.
Torulomyces
The genus Torulomyces was erected for two species (T. lagena and T. viscosus) which form dry connected chains in a basipetal manner (Delitsch 1943). Stolk & Samson (1983) transferred Torulomyces lagena, the type species, to Penicillium. This transfer was based on morphological similarities, such as the phialide shape and cultural appearances (Fig. 6). Later, Pitt & Samson (1993) did not accept this transfer to Penicillium, and Torulomyces was re-instated. Our phylogenetic data support Stolk & Samson's (1983) proposal to transfer Torulomyces to Penicillium and other species described in Torulomyces need to be combined with Penicillium.
Currently, eight species are described in Torulomyces: T. brunneus, T. indicus, T. laevis, T. lagena, T. macrosporus, T. ovatus, T. parviverrucosus and T. viscosus. Isolate CBS 185.65 was designated as the neotype of P. lagena, and Eupenicillium limoneum was considered to be the teleomorph of this species (Stolk & Samson 1983). Unfortunately, the ex-type culture of E. limoneum (CBS 650.82T) maintained in the CBS collection is dead. Stolk & Samson (1983) are followed here and E. limoneum is kept in synonymy with P. lagena. Delitsch's species Torulomyces viscosus remains doubtful since no type material is available and the diagnosis lacks critical details (Stolk & Samson 1983, Ando et al. 1998). No ex-type material of Torulomyces macrosporus could be obtained; based on its protologue (Matsushima 1987), T. macrosporum may belong to Monocillium (Ando et al. 1998).Torulomyces laevis, T. ovatus and T. parviverrucosus were described by Ando et al. (1998) and in the same publication Monocillium humicola var. brunneum was combined with T. brunneus. The type strain of T. brunneus CBS 382.64T is closely related to Torulomyces lagena CBS 185.65NT; these isolates have identical ITS sequences, but differ in their partial β-tubulin, calmodulin and RPB2 sequences (ITS 100 %; calmodulin 98.3 % and β-tubulin 98.4 % and RPB2 98.3 %; unpubl. data). Ando et al. (1998) is followed here and this species is kept as separate. No type material of T. laevis, T. ovatus and T. parviverrucosus was available for analysis, but a detailed study of the species descriptions suggests they warrant separate species status. New combinations in Penicillium are proposed below. Various isolates with similar morphology to P. lagena are maintained in the CBS collections (CBS 185.65, CBS 382.64, CBS 287.66, CBS 337.97, CBS 120415, CBS 110532, DTO 82A8, DTO 92D1), and preliminary sequencing results show a sequence variation among these strains, suggesting the presence of multiple species (unpubl. data). A thorough taxonomic study should be preformed to elucidate the species diversity in this clade.
The genus Monocillium needs further attention. This genus was established for a single species, M. indicum (Saksena 1955). Based on conidium morphogenesis, Hashmi et al. (1972) placed Monocillium in synonymy with Torulomyces, and later Kendrick & Carmichael (1973) made the combination Torulomyces indicus. However, a BLAST search with the ITS sequence of the type strain of M. indicum (UAMH 1499, GenBank GQ169328) showed that the closest relatives are among Hypocreaceae (Sigler et al. 2010). This is in agreement with Gams (1971), who showed that Monocillium species are anamorphs related to Niesslia species.
Part Three: sectional delimitation within Penicillium s. str.
Classification
Dierckx (1901) proposed the first infrageneric classification of Penicillium and introduced the subgenera Aspergilloides, Biverticillium and Eupenicillium (Biourge 1923). Biourge (1923) expanded this subdivision and accepted two subgenera, two sections, four series and six subsections. The sections Bulliardium (Asymetrica) was introduced by Biourge (1923) and in this section Penicillium species with branched conidiophores were included. No type species was designated and species with terverticillate conidiophores belong to Biourge's definition of his section Bulliardium (Asymetrica). We decided to synonymise this section with section Penicillium. The section Biverticillium belongs to Talaromyces s. str. and is not treated here (Fig. 1). In the classical work of Thom (1930: 155–159), Penicillium is divided in four subgenera (although not named as such), and 12 sections and 17 subsections. Raper & Thom (1949) introduced various new sections, subsections and series and Ramírez (1982) largely followed Raper and Thom's classification. Neither provided Latin descriptions for their newly introduced sections (and series), and these names are therefore regarded as nomen invalidum are not considered further here. Pitt (1980) divided Penicillium into four subgenera, 10 sections and 21 series. Five years later, Stolk & Samson (1985) proposed another taxonomic scheme for Penicillium anamorphs. In the latter taxonomic scheme, both sexual and asexual species were treated. More recently, Samson & Frisvad (2004) revised subgenus Penicillium and five sections and 17 series were recognised. An overview of sections and their type species of the studies of Thom (1930), Pitt (1980), Stolk & Samson (1985) and Frisvad & Samson (2004) is shown in Table 5.
Table 5
Overview of sectional classification in different studies of Penicillium
| Thom (1930) | Pitt (1980) | Stolk & Samson (1985) | Current study | ||||
|---|---|---|---|---|---|---|---|
| Section | Type species | Section | Type species | Section | Type species | Section | Type species |
| Ascogena | P. luteum | Aspergilloides | P. aurantiobrunneum | Aspergilloides | P. glabrum | Aspergilloides | P. aurantiobrunneum |
| Brevi-compacta | P. brevicompactum | Coremigenum | P. duclauxii | Biverticillium | P. minioluteum | Brevicompacta* | P. olsonii |
| Coremigena | P. duclauxii | Coronatum | P. olsonii | Coremigenum | P. duclauxii | Canescentia | P. canescens |
| Fasciculata | Fasiculate Penicillia e.g. P. hirsutum | Cylindrosporum | P. italicum | Divaricatum | P. janthinellum | Charlesii | P. charlesii |
| Funiculosa | Undefined; similar to Lanata-divaricata | Divaricatum | P. janthinellum | Eladia | P. sacculum | Chrysogena* | P. chrysogenum |
| Lanata-divaricata | P. janthinellum-type | Exilicaulis | P. restrictum | Geosmithia | P. lavendulum | Cinnamopurpurea | P. cinnamopurpureum |
| Lanata-typica | P. camemberti | Furcatum | P. oxalicum | Inordinate | P. arenicola | Citrina | P. citrinum |
| Luteo-virida | P. minioluteum | Inordinate | P. arenicola | Penicillium | P. expansum | Digitata* | P. digitatum |
| Miscellanea | Miscellaneous species and genera | Penicillium | P. expansum | Ramosum | P. lanosum | Eladia | P. sacculum |
| (Monoverticillata)-stricta | Undefined section | Simplicium | P. minioluteum | Torulomyces | P. lagena | Exilicaulis | P. restrictum |
| (Monoverticillata)-Ramigena | Citromyces species | Fasciculata* | P. viridicatum | ||||
| Velutina | Undefined section | Fracta | P. fractum | ||||
| Gracilenta | P. gracilentum | ||||||
| Lanata-divaricata | P. janthinellum | ||||||
| Ochrosalmonea | P. ochrosalmoneum | ||||||
| Paradoxa | A. paradoxus | ||||||
| Penicillium* | P. expansum | ||||||
| Ramigena | P. cyaneum | ||||||
| Ramosa | P. lanosum | ||||||
| Roguefortorum* | P. roqueforti | ||||||
| Sclerotiora | P. sclerotiorum | ||||||
| Stolkia | P. stolkiae | ||||||
| Thysanophora | S. glauco-albidum | ||||||
| Torulomyces | P. lagena | ||||||
| Turbata | P. turbatum | ||||||
The classification of Eupenicillium does not have such a long history: Pitt (1980) was the first, and introduced eight series. In the monograph of Stolk & Samson (1983), four sections were introduced for the grouping of the Eupenicillium species and Pitt's infrageneric concept of classifying species in series was abandoned.
Accepted species and their position in the sections of Penicillium
The phylogenetic relationship among Penicillium s. str. was studied using combined sequence data of four loci. Based on these results (Fig. 7), Penicillium is subdivided into two subgenera and 25 sections. An overview of these sections is presented in Table 5, together with the type species of each section. In our study, a new sectional subdivision is proposed and older names at different ranks (e.g. subgeneric, subsection and series names) and invalid names (Raper & Thom 1949, Ramírez 1982) are not considered. Assignment of the species to the various sections was mainly based on the overviews presented in Figs Figs88 and and10,10, ,11,11, ,12,12, ,1313 and other published molecular-based data. The accepted Penicillium and Eupenicillium species mentioned in the list of “accepted species and their synonyms in Trichocomaceae” (Pitt et al. 2000) were used as a starting point for dividing the species among the various sections, updated species described after 2000. In various cases, the same Penicillium and Eupenicillium species share the same ex-type specimen. However, if the type material of the Penicillium morph differs from the Eupenicillium morph, then both ex-type strains were included in the study and additional comments are given in the text.
Clade 1: section Aspergilloides
= Eupenicillium sect. Pinetorum (Pitt) Stolk & Samson, Stud. Mycol. 23: 88. 1983.
In: Penicillium subgenus Aspergilloides.
Type: Penicillium aurantiobrunneum Dierckx
Most members of this section grow quickly on agar media, form velvety colonies and are predominantly monoverticillate. This section corresponds to group 2 of Peterson (2000a). Two teleomorph species are positioned in this section: P. fuscum and P. saturniforme. Stolk (1968) found ascospores in an old culture of the type strain of P. pinetorum and described the ascosporic state as Eupenicillium pinetorum. Later, the anamorph of E. pinetorum was linked to P. fuscum (Stolk & Samson 1983); the latter name is older than P. pinetorum and therefore used here. The taxonomic position of P. lapidosum warrants further attention. Peterson (2000a) suggested that this species is conspecific with P. thomii. However, our results show that the type strain of this species (CBS 343.48T) is phylogenetically related to P. namyslowskii (Fig. 7, clade 10) and therefore unrelated to section Aspergilloides. Based on the data presented in Fig. 8 and literature (Peterson 2000a, Peterson & Horn 2009, Wang & Zhuang 2009, Barreto et al. 2011), we place the following species in section Aspergilloides:
Penicillium ardesiacum Novobranova, Novosti Sist. Nizs. Rast. 11: 228. 1974.
Penicillium asperosporum Smith, Trans. Br. Mycol. Soc. 48: 275. 1965.
Penicillium crocicola Yamamoto, Scient. Rep. Hyogo Univ. Agric., Agric. Biol. Ser. 2, 2: 28. 1956.
Penicillium fuscum (Sopp) Biourge, Cellule 33: 103. 1923 (Stolk & Samson 1983).
Penicillium georgiense Peterson & Horn, Mycologia 101: 79. 2009.
Penicillium glabrum (Wehmer) Westling, Ark. Bot. 11: 131. 1911 (syn. P. terlikowskii; Barreto et al. 2011).
Penicillium kananaskense Seifert, Frisvad & McLean, Can. J. Bot. 72: 20. 1994 (unpubl. data, K.A. Seifert).
Penicillium lapatayae Ramírez, Mycopathol. 91: 96. 1985 (Frisvad et al. 1990c).
Penicillium lividum Westling, Ark. Bot. 11: 134. 1911.
Penicillium montanense Christensen & Backus, Mycologia 54: 574. 1963.
Penicillium odoratum Christensen & Backus, Mycologia 53: 459. 1962 (this study, Fig. 8).
Penicillium palmense Ramírez & Martínez, Mycopathol. 66: 80. 1978.
Penicillium patens Pitt & Hocking, Mycotaxon 22: 197. 1985.
Penicillium quercetorum Baghdadi, Nov. Sist. Niz. Rast. 5: 110. 1968.
Penicillium saturniforme (Wang & Zhuang) Houbraken & Samson, Stud. Mycol. 70: 48. 2011 (this study).
Penicillium spinulosum Thom, Bull. Bur. Anim. Ind. U.S. Dep. Agric. 118: 76. 1910.
Penicillium subericola Barreto, Frisvad & Samson, Fungal Diversity 49: 32. 2011.
Penicillium thiersii Peterson, Bayer & Wicklow, Mycologia 96: 1283. 2004.
Penicillium thomii Maire, Bull. Soc. Hist. Nat. Afrique N. 8: 189. 1917.
Clade 2: section Sclerotiora Houbraken & Samson, sect. nov. MycoBank MB563124.
Sectio in Penicillio subgen. Aspergilloide. Mycelio saepe colorato, plus minusve flavido et/vel aurantiaco. Sclerotis/cleistotheciis claris. colore.
In: Penicillium subgenus Aspergilloides
Type: Penicillium sclerotiorum van Beyma
Members of section Sclerotiora generally have monoverticillate conidiophores; however, exceptions are P. malachiteum, P. nodositatum and P. herquei, which form symmetrically biverticillate conidiophores. The mycelium of members of sect. Sclerotiora is pigmented in shades of yellow and/or orange, reverse colony colours in shades of yellow, orange or red, and sclerotia and cleistothecia are, if present, bright coloured. Species belonging to this section occur regularly in and are abundant upon substrata exposed to soil. This section corresponds with group 3 of Peterson (2000a). Our list of species belonging to this section was composed based on the data presented in Fig. 8 and studies by Peterson (2000a), Peterson et al. (2003, 2004), Peterson & Horn (2009), Nonaka et al. (2011) and Rivera & Seifert (2011). Isolate NRRL 2060 is included in Fig. 8 and Peterson & Horn (2009) treated this strain as the type of P. multicolor. However, Raper & Thom's (1949) isolates of P. multicolor differ in significant features from the original description of Grigorieva-Manoilova & Poradielova (1915) (Pitt 1980), and Rivera & Seifert (2011) treated this species as a synonym of P. fellutanum. Penicillium nodositatum shares identical partial RPB2 sequences with P. bilaiae and might be conspecific with the latter species. More research is needed because the former species produces biverticillate conidiophores and the latter strictly monoverticillate structures (Pitt 1980, Valla et al. 1989).
Penicillium adametzii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 507. 1927.
Penicillium adametzioides Abe ex Smith, Trans. Br. Mycol. Soc. 46: 335. 1963.
Penicillium angulare Peterson, Bayer & Wicklow, Mycologia 96: 1289. 2004.
Penicillium bilaiae Chalabuda, Bot. Mater. Otd. Sporov. Rast. 6: 165. 1950.
Penicillium brocae Peterson, Pérez, Vega & Infante, Mycologia 95: 143. 2003.
Penicillium cainii Rivera & Seifert, Stud. Mycol. 70: 147. 2011.
Penicillium guanacastense Rivera, Urb & Seifert, Mycotaxon, in press. 2011.
Penicillium herquei Bainier & Sartory, Bull. Soc. Mycol. France 28: 121. 1912.
Penicillium hirayamae Udagawa, J. Agric. Sci. Tokyo Nogyo Daigaku 5: 6. 1959.
Penicillium jacksonii Rivera & Seifert, Stud. Mycol. 70: 151. 2011.
Penicillium johnkrugii Rivera & Seifert, Stud. Mycol. 70: 151. 2011.
Penicillium jugoslavicum Ramírez & Muntañola-Cvetkovic, Mycopathol. 88: 65. 1984.
Penicillium malachiteum (Yaguchi & Udagawa) Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium mallochii Rivera, Urb & Seifert Mycotaxon, in press. 2011.
Penicillium nodositatum Valla, Plant and Soil 114: 146. 1989.
Penicillium sclerotiorum van Beyma, Zentralbl. Bakteriol., 2. Abt., 96: 418. 1937.
Penicillium viticola Nonaka & Masuma, Mycoscience 52: 339. 2011.
Clade 3: section Charlesia Houbraken & Samson, sect. nov. MycoBank MB563125.
Sectio in Penicillio subgen. Aspergilloide. Solum in CYA, conidiophoris ad apicem inflatis.
In: Penicillium subgenus Aspergilloides
Type: Penicillium charlesii Smith
The phylogeny of this section was studied by Peterson et al. (2005). In the same study, an overview was presented of phenotypic characters to differentiate species within section Charlesii. It was stated that the overall phenotypic similarity of these species is striking; however, no shared characters were given. With exception of P. indicum, all members of section Charlesii grow restricted on CYA and have conidiophores with an apical swelling. Species of this section can be strictly monoverticillate, but P. charlesii and P. fellutanum can also be irregularly biverticillate. Included species are based on the data presented in Fig. 8 and Peterson (2000a) and Peterson et al. (2005).
Penicillium charlesii Smith, Trans. Br. Mycol. Soc. 18: 90. 1933.
Penicillium coffeae Peterson, Vega, Posada & Nagai, Mycologia 97: 662. 2005.
Penicillium fellutanum Biourge, Cellule 33: 262. 1923.
Penicillium georgiense Peterson & Horn, Mycologia 101: 79. 2009.
Penicillium indicum Sandhu & Sandhu, Can. J. Bot. 41: 1273. 1963 (syn. P. gerundense, Peterson & Horn 2009).
Penicillium phoeniceum van Beyma, Zentralbl. Bakteriol., 2. Abt., 88: 136. 1933.
Clade 4: section Thysanophora Houbraken & Samson, sect. nov. MycoBank MB563126.
Sectio in Penicillio subgen. Aspergilloide. Coloniis pullis, conidiophoris pigmentatis, compactis et incremento secundario stipitis per proliferationem penicillii apicali.
In: Penicillium subgenus Aspergilloides
Type: Sclerotium glauco-albidum Desmazières
The genus Thysanophora is placed in synonymy with Penicillium (see above). The section is characterised by the formation dark coloured colonies, pigmented and stout conidiophores and the majority of species have secondary growth of the stipe by means of the proliferation of an apical penicillius. Nine specific epithets have been combined with Thysanophora, and eight are accepted species. Mercado-Sierra et al. (1998) is largely followed here and the following species belong in section Thysanophora:
Penicillium asymmetricum (Subramanian & Sudha) Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium coniferophilum Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium glaucoalbidum (Desmazières) Houbraken & Samson, Stud. Mycol.70: 47. 2011 (this study).
Penicillium hennebertii Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium longisporum (Kendrick) Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium melanostipe Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium taiwanense (Matsushima) Houbraken & Samson, Stud. Mycol. 70: 48. 2011 (this study).
Penicillium taxi Schneider, Zentralblatt für Bakteriologie und Parasitenkunde, Abteilung 2, 110: 43. 1956.
Clade 5: section Ochrosalmonea Houbraken & Samson, sect. nov. MycoBank MB563127.
Sectio in Penicillio subgen. Aspergilloide. Mycelio conspicue pigmentoso, flavido; phialidibus ampulliformibus vel acerosis; conidiis apiculatis.
In: Penicillium subgenus Aspergilloides
Type: Penicillium ochrosalmoneum Udagawa
Penicillium ochrosalmoneum and P. isariiforme are accommodated in section Ochrosalmonea (Fig. 5, clade 5). Both species seem macroscopically dissimilar. Penicillium isariiforme grows quickly on agar media MEA and CYA (Pitt 1980) and forms characteristic feather-like synnemata (Samson et al. 1976, Fig. 9). In contrast, P. ochrosalmoneum isolates grow slowly on agar media and forms a velutinous colony surface (Pitt 1980). However, both species form conspicuous yellow coloured mycelium, ampulliform to acerose shaped phialides and apiculate conidia. The classification of P. isariiforme in Penicillium was subject of various studies. This species was classified in subgenus Biverticillium (= Talaromyces s. str.) (Pitt 1980, Frisvad & Filtenborg 1983), but also in subgenus Penicillium (= Penicillium s. str.) (Ramírez 1982, Samson et al. 1976). Figure 7 shows that P. isariiforme phylogenetically belongs to subgenus Aspergilloides in Penicillium s. str.
Penicillium isariiforme CBS 247.56. A. Colonies grown for 14 d at 25 °C, from left to right: MEA, YES, CYA. B–D. Conidiophores. E. Conidia. Scale bar = 10 μm.
The holotype of Eup. ochrosalmoneum is CBS 489.66 and CBS 231.60 is the ex-type of P. ochrosalmoneum. The strains share identical partial RPB2 sequences and therefore E. ochrosalmoneum is regarded as conspecific with P. ochrosalmoneum (Fig. 12). Based on the data presented in Fig. 12, the following species belong in section Ochrosalmonea.
Penicillium isariiforme Stolk & Meyer, Trans. Br. Mycol. Soc. 40: 187. 1957.
Penicillium ochrosalmoneum Udagawa, J. Agric. Sci. Tokyo Nogyo Daigaku 5: 10. 1959.
Clade 6: section Cinnamopurpurea Houbraken & Samson, sect. nov. MycoBank MB563128.
Sectio in Penicillio subgen. Aspergilloide. Sect. Ornatis similis, sed conidiophoris semper simplicibus vel biverticillate divaricates; stipitibus cum conidiophoris distincte vesiculosis.
In: Penicillium subgenus Aspergilloides
Type: Penicillium cinnamopurpureum Udagawa
Members of section Cinnamopurpurea grow slowly on MEA and CYA and can be strictly monoverticillate, but species with biverticillate conidiophores are also present in this section. The majority of the species have distinct vesicular conidiophores. This section is phenotypically related to section Ornata; however, statistical support for this relationship is lacking in our phylogenetic analysis (Fig. 7).
Penicillium cinnamopurpureum was originally described by Abe (1956) without a Latin diagnosis, and validated by Udagawa (1959). Stolk & Samson (1983) considered P. dierckxii the anamorph of Eupenicillium cinnamopurpureum and Pitt (1980) linked P. phoeniceum to E. cinnamopurpureum. Our data show that P. phoeniceum (sect. Charlesii, Fig. 8) and P. dierckxii (sect. Ramigena, Fig. 10) are phylogenetically distinct from P. cinnamopurpureum. Furthermore, partial RPB2 data show that the type strains of P. cinnamopurpureum (CBS 847.68) and E. cinnamopurpureum (CBS 490.66) are similar (Fig. 10).
Penicillium chermesinum is also placed in this section. This species was neotypified with NRRL 2048 (= CBS 231.81), because the type culture, NRRL 735, no longer adequately represented Biourge's protologue (Pitt 1980). Molecular analysis shows that these two species are phylogenetically unrelated. The ITS-partial 28S rDNA sequences of NRRL 735T (= GenBank no. AF033413) is related to P. cinnamopurpureum (Peterson 2000a) while the neotype of this species, NRRL 2048NT, (AY742693) is related to P. indicum in section Charlesii. Based on the data presented in Fig. 10 and Peterson & Horn (2009), the following species are accommodated in Cinnamopurpurea.
Penicillium chermesinum Biourge, Cellule 33: 284. 1923.
Penicillium cinnamopurpureum Udagawa, J. Agric. Food Sci., Tokyo 5: 1. 1959.
Penicillium ellipsoideosporum Wang & Kong, Mycosystema 19: 463. 2000.
Penicillium idahoense Paden, Mycopath. Mycol. Appl. 43: 261. 1971 (Peterson & Horn 2009, this study).
Penicillium incoloratum Huang & Qi, Acta Mycol. Sin. 13: 264. 1994.
Penicillium malacaense Ramírez & Martínez, Mycopathologia 72: 186. 1980 (syn. P. ovetense, this study) (Peterson & Horn 2009).
Penicillium nodulum Kong & Qi, Mycosystema 1: 108. 1988.
Penicillium parvulum Peterson & Horn, Mycologia 101: 75. 2009.
Penicillium shennangjianum Kong & Qi, Mycosystema 1: 110. 1988.
Clade 7: section Ramigena Thom, The Penicillia: 225. 1930. In: Penicillium subgenus Aspergilloides
Type: Penicillium cyaneum (Bainier & Sartory) Biourge
This section is based on Thom's section Ramigena. Thom (1930) introduced this section for species where monoverticillate conidiophores are evident, but divaricate branching at various levels without a definiteness of organisation or arrangement is consistently observed. Most species illustrated by Banier & Sartory (1913) as species of Citromyces are accommodated in this section (fide Thom 1930). Members of the section Ramigena share the following characters: a slow growth rate on agar media, a monoverticillate branching system with non-vesiculate stipes. Conidia are relatively large (3–4 μm), smooth and ellipsoidal or pyriform (Pitt 1980). Penicillium ornatum is the sole member known in this section with a teleomorph (Udagawa 1968, Pitt 1980). The ascospores of this species are ornamented with two and sometimes four longitudinal flanges. The ex-type culture of P. implicatum in the CBS collection (CBS 232.38) is a Penicillium citrinum, and therefore this species is not accepted as distinct (Frisvad et al. 1990b, Houbraken et al. 2010b). Pitt (1980) neotypified P. implicatum with CBS 184.81 and Fig. 10 shows that this strain is closely related to the type of Penicillium hispanicum CBS 691.77. This neotypification is not accepted here and P. implicatum sensu Pitt is considered as a synonym of P. hispanicum. Pitt et al. (2000) accepted P. dierckxii, P. cyaneum and P. sublateritium as single species in their overview of accepted species in Penicillium. This concept is followed here; however, partial RPB2 data (Fig. 10) shows that these three species are very closely related and might represent one species.
Penicillium capsulatum Raper & Fennell, Mycologia 40: 528. 1948.
Penicillium cyaneum (Bainier & Sartory) Biourge, Cellule 33: 102. 1923.
Penicillium dierckxii Biourge, Cellule 33: 313. 1923.
Penicillium hispanicum Ramírez, Martínez & Ferrer, Mycopathol. 66: 77. 1978 (syn. Penicillium implicatum sensu Pitt).
Penicillium ornatum Udagawa, Trans. Mycol. Soc. Japan 9: 49.1968.
Penicillium ramusculum Batista & Maia, Anais Soc. Biol. Pernamb. 13: 27. 1955 (syn. P. brevissimum Rai & Wadhwani) (this study, Peterson & Horn 2009).
Penicillium sublateritium Biourge, Cellule 33: 315. 1923.
Clade 8: section Torulomyces (Delitsch) Stolk & Samson, Adv. Pen. Asp. Syst.: 169. 1985.
In: Penicillium subgenus Aspergilloides
Type: Penicillium lagena (Delitsch) Stolk & Samson
The genus Torulomyces is synonymised with Penicillium and consequently the majority of the species described in Torulomyces are transferred to Penicillium (this study). Figure 7 shows that P. lagena is related to P. cryptum and P. lassenii. These species have a slow growth rate on the agar media CYA and MEA and form short-stiped monoverticillate or terminal biverticillate conidiophores. Phialides are predominantly singly formed in P. lagena, short, 4–7 μm long, with a narrowed base and a swollen middle that tapers abruptly into a narrow neck (Fig. 6).
Penicillium cryptum Gochenaur, Mycotaxon 26: 349. 1986.
Penicillium lagena (Delitsch) Stolk & Samson, Stud. Mycol. 23:100. 1983.
Penicillium laeve (K. Ando & Manoch) Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium lassenii Paden, Mycopathol. Mycol. Appl. 43: 266. 1971.
Penicillium ovatum (K. Ando & Nawawi) Houbraken & Samson, Stud. Mycol. 70: 48. 2011 (this study).
Penicillium parviverrucosum (K. Ando & Pitt) Houbraken & Samson, Stud. Mycol. 70: 48. 2011 (this study).
Penicillium porphyreum Houbraken & Samson, Stud. Mycol. 70: 48. 2011 (this study).
Clade 9: section Fracta Houbraken & Samson, sect. nov. MycoBank MB563129.
Sectio in Penicillio subgen. Aspergilloide. Coloniis in agaro tarde crescentibus; ascosporis spinulosis; phialidibus ampullifomibus vel lanceolatis; conidiis ellipsoideis.
In: Penicillium subgenus Aspergilloides
Type: Penicillium ornatum Udagawa
Penicillium inusitatum and P. fractum belong to section Fracta and both are able to form a teleomorph. Pitt (1980) noted that these two species are closely related, differing principally in conidiophore structure. Both species share unusual ascospore morphology for Penicillium species: the ascospores are spheroidal without flanges or furrows and ornamented by spines. Furthermore, both species grow slowly on agar media, form ampulliform to lanceolate phialides and ellipsoidal conidia. Phylogenetically, section Fracta might be related to section Torulomyces (72 % bs, < 0.95 pp). However, ascospores produced by the members of the latter section have two ridges (P. lagena, P. lassenii, P. cryptum).
Penicillium fractum Udagawa, Trans. Mycol. Soc. Japan 9: 51. 1968.
Penicillium inusitatum Scott, Mycopathol. Mycol. Appl. 36: 20. 1968.
Clade 10: section Exilicaulis Pitt, The Genus Penicillium: 205. 1980.
In: Penicillium subgenus Aspergilloides
Type: Penicillium restrictum Gilman & Abbott
= Eupenicillium section Lapidosa (Pitt) Stolk & Samson, Stud. Mycol. 23: 55. 1983.
Pitt (1980) defined section Exilicaulis for monoverticillate species with stipes lacking a terminal vesicular swelling. The phylogenetic delimitation is broader and also several species with an additional branch are included (e.g. P. raciborski, P. melinii, P. velutinum, P. corylophilum). This section largely corresponds with group 4 of Peterson (2000a); the only difference is that Peterson placed P. turbatum in this clade, while our data shows that this species belongs to section Turbata (group 6 fide Peterson (2000a)). Based on Fig. 10 and data of Peterson et al. and Peterson 2000a, the following species are included in section Exilicaulis:
Penicillium alutaceum Scott, Mycopathol. Mycol. Appl. 36: 17. 1968.
Penicillium atrosanguineum Dong, Ceská Mycol. 27: 174. 1973.
Penicillium burgense Quintanilla, Avances Nutr. Mejora Anim. Aliment. 30: 176. 1990.
Penicillium catenatum Scott, Mycopathol. Mycol. Appl. 36: 24. 1968.
Penicillium chalybeum Pitt & Hocking, Mycotaxon 22: 204. 1985.
Penicillium cinerascens Biourge, Cellule 33: 308. 1923.
Penicillium cinereoatrum Chalabuda, Bot. Mater. Otd. Sporov. Rast. 6: 167, 1950 (Frisvad et al. 1990c).
Penicillium citreonigrum Dierckx, Ann. Soc. Sci. Bruxelles 25: 86. 1901.
Penicillium corylophilum Dierckx, Ann. Soc. Sci. Bruxelles 25: 86. 1901.
Penicillium decumbens Thom, Bull. Bur. Anim. Ind. U.S. Dep. Agric. 118: 71. 1910.
Penicillium dimorphosporum Swart, Trans. Br. Mycol. Soc. 55: 310. 1970.
Penicillium dravuni Janso, Mycologia 97: 445. 2005.
Penicillium erubescens Scott, Mycopathol. Mycol. Appl. 36: 14. 1968.
Penicillium fagi Ramírez & Martínez, Mycopathol. 63: 57. 1978.
Penicillium flavidostipitatum Ramírez & González, Mycopathol. 88: 3. 1984 (preliminary sequencing results show that this species is closely related to P. namyslowskii).
Penicillium guttulosum Gilman & Abbott, Iowa State Coll. J. Sci. 1: 298. 1927 (Peterson et al. 2011).
Penicillium heteromorphum Kong & Qi, Mycosystema 1: 107. 1988.
Penicillium katangense Stolk, Ant. van Leeuwenhoek 34: 42. 1968.
Penicillium lapidosum Raper & Fennell, Mycologia 40: 524. 1948.
Penicillium maclennaniae Yip, Trans. Br. Mycol. Soc. 77: 202. 1981.
Penicillium melinii Thom, Penicillia: 273. 1930.
Penicillium menonorum Peterson, IMA Fungus 2: 122. 2011.
Penicillium meridianum Scott, Mycopathol. Mycol. Appl. 36: 12. 1968.
Penicillium namyslowskii Zaleski, Bull. Int. Aead. Polonc. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 479. 1927.
Penicillium nepalense Takada & Udagawa, Trans. Mycol. Soc. Japan 24: 146. 1983.
Penicillium parvum Raper & Fennell, Mycologia 40: 508. 1948 (this study).
Penicillium philippinense Udagawa & Y. Horie, J. Jap. Bot. 47: 341. 1972.
Penicillium pimiteouiense Peterson, Mycologia 91: 271. 1999.
Penicillium raciborskii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 454. 1927.
Penicillium restrictum Gilman & Abbott, Iowa State Coll. J. Sci. 1: 297. 1927.
Penicillium rubefaciens Quintanilla, Mycopathol. 80: 73. 1982.
Penicillium rubidurum Udagawa & Horie, Trans. Mycol. Soc. Japan 14: 381. 1973.
Penicillium smithii Quintanilla, Avances Nutr. Mejora Anim. Aliment. 23: 340. 1982 (syn. P. corynephorum, P. sabulosum).
Penicillium striatisporum Stolk, Ant. van Leeuwenhoek 35: 268. 1969.
Penicillium terrenum Scott, Mycopathol. Mycol. Appl. 36: 1. 1968.
Penicillium toxicarium Miyake, Rep. Res. Inst. Rice Improvement 1: 1. 1940 (nom. inval., Art. 36) (Serra et al. 2008).
Penicillium velutinum van Beyma, Zentralbl. Bakteriol., 2. Abt., 91: 353. 1935.
Penicillium vinaceum Gilman & Abbott, Iowa State Coll. J. Sci. 1: 299. 1927.
Clade 11: Section Lanata-divaricata Thom, The Penicillia: 328. 1930.
= section Funiculosa Thom, The Penicillia: 358. 1930.
= section Divaricatum Pitt, The Genus Penicillium: 238. 1980.
= section Furcatum Pitt, The Genus Penicillium: 272. 1980.
= Eupenicillium section Javanica (Pitt) Stolk & Samson, Stud. Mycol. 23: 55. 1983.
In: Penicillium subgenus Aspergilloides
Type: Penicillium janthinellum Biourge
Most of the species, but not all, of section Lanata-divaricata grow rapidly and form broadly spreading colonies. The majority of the species belonging to this section are strongly divaricate and the metulae are born terminally, subterminally and in intercalary positions, and in the latter case intergrading with monoverticillate conidiophores. Furthermore, the terminal cluster often consists of a prolongation of the main axis. Species belonging to section Lanata-divaricata are mainly soil inhabitants, but may also occur on leaf litter and vegetable remains in the later stage of decomposition (Raper & Thom 1949, Houbraken et al. 2011c). Many species of this section are unusually tolerant for heavy metals and some species have been proposed as efficient biosorbent agents in the bioleaching of zinc oxide, copper, lead and nickel (Burgstaller et al. 1992, Valix et al. 2001, Li et al. 2008).
Section Funiculosa is placed in synonymy with this section. Thom (1930) already noted that species belonging section Funiculosa have affinity with members of section Lanata-typica and that separation is hard to define. This observation is supported by our data: many species mentioned in Thom's section Funiculosa belong to section Lanata-divaricata. Raper & Thom's (1949) subsection Divaricata largely corresponds with our section Lanata-divaricata. They noted that members of their subsection have a definite relationship to Penicillium javanicum. Stolk & Samson (1983) also discussed this relationship and they placed 26 species in synonymy with Eupenicillium javanicum and P. simplicissimum. Recently, a phylogenetic study showed that many of these synonyms should be treated as separate species (Peterson 2000a, Houbraken et al. 2011c). This section largely corresponds with Peterson's (2000a) group 5 and the list provided here for this section is mainly based on this data supplemented with data of Houbraken et al. (2011c). Penicillium cluniae, P. griseopurpureum and P. glaucoroseum were not included in these studies, though unpublished data shows that these three species also belong to this section.
The typification of P. brefeldianum, P. javanicum, P. levitum and P. ehrlichii warrants further attention. Dodge (1933) described P. brefeldianum as a holomorphic species. Pitt (1980) did not accept teleomorph species in Penicillium and a neotype (CBS 233.81 = FRR 71 = IMI 216895) was selected because the original type culture of P. brefeldianum distributed by Dodge no longer produced cleistothecia. Subsequently, Dodge's strain (CBS 235.81 = FRR 710 = IMI 216896 = NRRL 710) was used for the description of the anamorph of Eupenicillium brefeldianum (as Penicillium dodgei). Teleomorphs are allowed in Penicillium and therefore Dodge's P. brefeldianum is re-instated. Furthermore, Fig. 11 shows that Dodge's type strain (CBS 235.81) differs from Pitt's neotype (CBS 233.81) and this neotype is similar to the type of P. caperatum (CBS 443.75T). Penicillium levitum, P. javanicum and P. ehrlichii were described including a teleomorph. Pitt (1980) introduced the new species names P. rasile, P. indonesiae and P. klebahnii respectively, for the anamorphs of P. levitum, P. javanicum and P. ehrlichii. These names are not used here for the same the reason as mentioned under P. brefeldianum.
Penicillium abidjanum Stolk, Ant. van Leeuwenhoek 34: 49. 1968.
Penicillium araracuarense Houbraken, C. López-Q, Frisvad & Samson, Int. J. Syst. Evol. Microbiol. 61: 1469. 2011.
Penicillium brasilianum Batista, Anais Soc. Biol. Pernambuco 15: 162. 1957.
Penicillium brefeldianum Dodge, Mycologia 25: 92. 1933 (syn. P. dodgei).
Penicillium caperatum Udagawa & Horie, Trans. Mycol. Soc. Japan 14: 371. 1973 (syn. E. brefeldianum sensu Pitt).
Penicillium cluniae Quintanilla, Avances Nutr. Mejora Anim. Aliment. 30: 174. 1990. (unpubl. data)
Penicillium coeruleum Sopp apud Biourge, Cellule 33: 102. 1923.
Penicillium cremeogriseum Chalabuda, Bot. Mater. Otd. Sporov. Rast. 6: 168. 1950.
Penicillium daleae Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 495. 1927.
Penicillium ehrlichii Klebahn, Ber. Deutsch. Bot. Ges. 48: 374. 1930.
Penicillium elleniae Houbraken, C. López-Q, Frisvad & Samson, Int. J. Syst. Evol. Microbiol. 61: 1470. 2011.
Penicillium glaucoroseum Demelius, Verh. Zool.-Bot. Ges. Wien 72: 72. 1923. (unpubl. data)
Penicillium griseopurpureum Smith, Trans. Br. Mycol. Soc. 48: 275. 1965 (unpubl. data).
Penicillium janthinellum Biourge, Cellule 33: 258. 1923.
Penicillium javanicum van Beyma, Verh. Kon. Ned. Akad. Wetensch., Afd. Natuurk., Tweede Sect., 26: 17. 1929 (syn. P. oligosporum, P. indonesiae).
Penicillium levitum Raper & Fennell, Mycologia 40: 511. 1948 (syn. P. rasile).
Penicillium limosum Ueda, Mycoscience 36: 451. 1995.
Penicillium lineolatum Udagawa & Horie, Mycotaxon 5: 493. 1977.
Penicillium ludwigii Udagawa, Trans. Mycol. Soc. Japan 10: 2. 1969.
Penicillium mariaecrucis Quintanilla, Avances Nutr. Mejora Anim. Aliment. 23: 334. 1982.
Penicillium meloforme Udagawa & Horie, Trans. Mycol. Soc. Japan 14: 376. 1973.
Penicillium ochrochloron Biourge, Cellule 33: 269. 1923.
Penicillium onobense Ramírez & Martínez, Mycopathol. 74: 44. 1981.
Penicillium oxalicum Currie & Thom, J. Biol. Chem. 22: 289. 1915.
Penicillium paraherquei Abe ex Smith, Trans. Br. Mycol. Soc. 46: 335. 1963.
Penicillium penarojense Houbraken, C. López-Q, Frisvad & Samson, Int. J. Syst. Evol. Microbiol. 61: 1471. 2011.
Penicillium piscarium Westling, Ark. Bot. 11: 86. 1911.
Penicillium pulvillorum Turfitt, Trans. Br. Mycol. Soc. 23: 186. 1939 (Syn. P. ciegleri).
Penicillium raperi Smith, Trans. Br. Mycol. Soc. 40: 486. 1957.
Penicillium reticulisporum Udagawa, Trans. Mycol. Soc. Japan 9: 52. 1968. (syn. P. arvense).
Penicillium rolfsii Thom, Penicillia: 489. 1930.
Penicillium simplicissimum (Oudemans) Thom, Penicillia: 335. 1930.
Penicillium skrjabinii Schmotina & Golovleva, Mikol. Fitopatol. 8: 530. 1974.
Penicillium svalbardense Frisvad, Sonjak & Gunde-Cimerman, Ant. van Leeuwenhoek 92: 48. 2007.
Penicillium vanderhammenii Houbraken, C. López-Q, Frisvad & Samson, Int. J. Syst. Evol. Microbiol. 61: 1473. 2011.
Penicillium vasconiae Ramírez & Martínez, Mycopathol. 72: 189. 1980.
Penicillium wotroi Houbraken, C. López-Q, Frisvad & Samson, Int. J. Syst. Evol. Microbiol. 61: 1474. 2011.
Penicillium zonatum Hodges & Perry, Mycologia 65: 697. 1973.
Clade 12: section Stolkia Houbraken & Samson, sect. nov. MycoBank MB563130.
Sectio in Penicillio subgen. Aspergilloide. Conidiophoris pigmentatis, metulis subapicalibus sympodialiter proliferantibus; phialidibus nullis.
In: Penicillium subgenus Aspergilloides
Type: Penicillium stolkiae Scott
Brown conidiophores occur in two phylogenetic unrelated sections of Penicillium s. str. One includes species belonging to section Thysanophora (previously assigned to the genus Thysanophora) (Iwamoto et al. 2002, Peterson & Sigler 2002) and the second lineage is centered around P. stolkiae, another species with conidiophores that also may be hyaline to definitely brown (Stolk & Samson 1983). Peterson & Sigler (2002) described four species with darkly melanised conidiophores, which are all closely related to P. stolkiae, namely P. subarticum, P. canariense, P. pullum and P. boreae. None of these species demonstrate the sympodial proliferation of subapical metulae and phialides present in section Thysanophora. The following species are placed in section Stolkia based on the data presented in Fig. 11 and of Peterson & Sigler (2002).
Penicillium boreae Peterson & Sigler, Mycol. Res. 106: 1112. 2002.
Penicillium canariense Peterson & Sigler, Mycol. Res. 106: 1113. 2002.
Penicillium donkii Stolk, Persoonia 7: 333. 1973.
Penicillium pullum Peterson & Sigler, Mycol. Res. 106: 1115. 2002.
Penicillium stolkiae Scott, Mycopathol. Mycol. Appl. 36: 8. 1968.
Penicillium subarcticum Peterson & Sigler, Mycol. Res. 106: 1116. 2002.
Clade 13: section Gracilenta Houbraken & Samson, sect. nov. MycoBank MB563131.
Sectio in Penicillio subgen. Aspergilloide. Coloniis 37 °C haud crescentibus, reverso olivaceo-brunneo vel brunneo, conidiis saepe late ellipsoideis vel ellipsoideis.
In: Penicillium subgenus Aspergilloides
Type: Penicillium gracilentum Udagawa & Horie
Four species are placed in section Gracilenta. Comparison of the phenotypic characters did not reveal many significant similarities among these species. All species did not grow at 37 °C and have an olive-brown to brown reverse on agar media. With exception of P. macrosclerotiorum, all species produced broadly ellipsoidal to ellipsoidal conidia (Abe 1956, Udagawa & Horie 1973, Pitt 1980, Takada & Udagawa 1983, Wang et al. 2007). The taxonomy and phylogeny of these species is not well studied and future research might reveal more shared characters.
Penicillium angustiporcatum Takada & Udagawa, Trans. Mycol. Soc. Japan 24: 143. 1983.
Penicillium estinogenum Komatsu & Abe ex Smith, Trans. Br. Mycol. Soc. 46: 335. 1963.
Penicillium macrosclerotiorum Wang, Zhang & Zhuang, Mycol. Res. 111: 1244. 2007.
Penicillium gracilentum Udagawa & Horie, Trans. Mycol. Soc. Japan 14: 373. 1973.
Clade 14: section Citrina Houbraken & Samson, sect. nov. MycoBank MB563132.
Sectio in Penicillio subgen. Aspergilloide. Formatione conidiophorum symmetricorum biverticillatorum.
In: Penicillium subgenus Aspergilloides
Type: Penicillium citrinum Thom
Species of section Citrina are commonly occurring in soil and the majority of the species form symmetrical biverticillate conidiophores. This section corresponds with group 1 of Peterson (2000a). The taxonomy of section Citrina is recently revised by Houbraken et al. (2010b, 2011b) and based on this data and Fig. 12, the following species are placed in section Citrina:
Penicillium anatolicum Stolk, Ant. van Leeuwenhoek 34: 46. 1968.
Penicillium argentinense Houbraken, Frisvad & Samson, Stud. Mycol. 70: 78. 2011.
Penicillium atrofulvum Houbraken, Frisvad & Samson, Stud. Mycol. 70: 80. 2011.
Penicillium aurantiacobrunneum Houbraken, Frisvad & Samson, Stud. Mycol. 70: 80. 2011.
Penicillium cairnsense Houbraken, Frisvad & Samson, Stud. Mycol. 70: 83. 2011.
Penicillium christenseniae Houbraken, Frisvad & Samson, Stud. Mycol. 70: 85. 2011.
Penicillium chrzaszczii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 464. 1927.
Penicillium citrinum Thom, Bull. Bur. Anim. Ind. U.S. Dep. Agric. 118: 61. 1910.
Penicillium copticola Houbraken, Frisvad & Samson, Stud. Mycol. 70: 88. 2011.
Penicillium cosmopolitanum Houbraken, Frisvad & Samson, Stud. Mycol. 70: 91. 2011.
Penicillium decaturense Peterson, Bayer & Wicklow, Mycologia 96: 1290. 2004.
Penicillium euglaucum van Beyma, Ant. van Leeuwenhoek 6: 269. 1940.
Penicillium galliacum Ramírez, Martínez & Berenguer, Mycopathol. 72: 30. 1980.
Penicillium godlewskii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 466. 1927.
Penicillium gorlenkoanum Baghdadi, Nov. Sist. Niz. Rast. 5: 97. 1968.
Penicillium hetheringtonii Houbraken, Frisvad & Samson, Fung. Div. 44: 125. 2010.
Penicillium manginii Duché & Heim, Trav. Cryptog. Louis L. Mangin: 450. 1931 (syn. P. pedemontanum, Houbraken et al. 2011b).
Penicillium miczynskii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 482. 1927.
Penicillium neomiczynskii Cole, Houbraken, Frisvad & Samson, Stud. Mycol. 70: 105. 2011.
Penicillium nothofagi Houbraken, Frisvad & Samson, Stud. Mycol. 70: 105. 2011.
Penicillium pancosmium Houbraken, Frisvad & Samson, Stud. Mycol. 70: 108. 2011.
Penicillium pasqualense Houbraken, Frisvad & Samson, Stud. Mycol. 70: 108. 2011.
Penicillium paxilli Bainier, Bull. Soc. Mycol. France 23: 95. 1907.
Penicillium quebecense Houbraken, Frisvad & Samson, Stud. Mycol. 70: 111. 2011.
Penicillium raphiae Houbraken, Frisvad & Samson, Stud. Mycol. 70: 114. 2011.
Penicillium roseopurpureum Dierckx, Ann. Soc. Sci. Bruxelles 25: 86. 1901.
Penicillium sanguifluum (Sopp) Biourge, La Cellule 33: 105. 1923. Penicillium shearii Stolk & Scott, Persoonia 4: 396. 1967.
Penicillium sizovae Baghdadi, Novosti Sist. Nizs. Rast. 1968: 103. 1968.
Penicillium steckii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 469. 1927.
Penicillium sumatrense Szilvinyi, Archiv. Hydrobiol. 14, Suppl. 6: 535. 1936.
Penicillium terrigenum Houbraken, Frisvad & Samson, Stud. Mycol. 70: 125. 2011.
Penicillium tropicoides Houbraken, Frisvad & Samson, Fung. Div. 44: 127. 2010.
Penicillium tropicum Houbraken, Frisvad & Samson, Fung. Div. 44: 129. 2010.
Penicillium ubiquetum Houbraken, Frisvad & Samson, Stud. Mycol. 70: 127. 2011.
Penicillium vancouverense Houbraken, Frisvad & Samson, Stud. Mycol. 70: 131. 2011.
Penicillium waksmanii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 468. 1927.
Penicillium wellingtonense Cole, Houbraken, Frisvad & Samson, Stud. Mycol. 70: 133. 2011.
Penicillium westlingii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 473. 1927.
Clade 15: Section Fasciculata Thom, The Penicillia: 374. 1930.
= Section Lanata-typica Thom, The Penicillia: 305. 1930.
= Section Viridicata Frisvad & Samson, Stud. Mycol. 49: 27. 2004.
In: Penicillium subgenus Penicillium
Type: Penicillium hirsutum Dierckx
Sections Lanata-typica and Viridicata are placed in synonymy with section Fasciculata. Lanata-typica was erected for species with vegetative aerial mycelium consisting of lanose, cottony or floccose colonies and only a small portion of the species currently present this section produce such structures (P. camemberti, P. commune, P. caseifulvum). Most species of section Fasciculata have a granulose or fasciculate colony texture and therefore the name Fasciculata is given priority to Lanata-typica. The current definition of Fasciculata is similar to that of Viridicata (Frisvad & Samson 2004). All species grow rather quickly, except species in series Verrucosa, which grow slowly. Most species this section have globose conidia and rough-walled conidiophore stipes. All species are psychrotolerant and grow well at low water activities (Frisvad & Samson 2004). Frisvad & Samson (2004) accommodated 28 species in section Viridicata (= Fasciculata). We excluded P. atramentosum from this section and placed this species in section Paradoxa. This species was placed in section Fasciculata based on its ability to grow on creatine as sole nitrogen source and its occurrence on cheese. However, Frisvad & Samson (2004) also noted that its ability to grow at very high pH values and the formation of smooth-walled stipes sets it apart from section Fasciculata. Penicillium osmophilum is tentatively accommodated in section Viridicata. Figure 13 shows that this species is most closely related to this section, but bootstrap support is lacking.
Penicillium albocoremium (Frisvad) Frisvad, Int. Mod. Tax. Meth. Pen. Asp. Clas.: 275. 2000.
Penicillium allii Vincent & Pitt, Mycologia 81: 300. 1989.
Penicillium aurantiogriseum Dierckx, Ann. Soc. Scient. Brux. 25: 88. 1901.
Penicillium camemberti Thom, Bull. Bur. Anim. Ind. USDA 82: 33. 1906.
Penicillium caseifulvum Lund, Filt. & Frisvad, J. Food Mycol. 1: 97. 1998.
Penicillium cavernicola Frisvad & Samson, Stud. Mycol. 49: 31. 2004.
Penicillium commune Thom, Bull. Bur. Anim. Ind. USDA 118: 56. 1910.
Penicillium crustosum Thom, Penicillia: 399. 1930.
Penicillium cyclopium Westling, Ark. Bot. 11: 90. 1911.
Penicillium discolor Frisvad & Samson, Ant. Van Leeuwenhoek, 72: 120. 1997.
Penicillium echinulatum Fassatiová, Acta Univ. Carol. Biol. 12: 326. 1977.
Penicillium freii Frisvad & Samson, Stud. Mycol. 49: 28. 2004.
Penicillium hirsutum Dierckx, Ann. Soc. Scient. Brux. 25: 89. 1901.
Penicillium hordei Stolk, Ant. van Leeuwenhoek 35: 270. 1969.
Penicillium melanoconidium (Frisvad) Frisvad & Samson, Stud. Mycol. 49: 28. 2004.
Penicillium neoechinulatum (Frisvad, Filt. & Wicklow) Frisvad & Samson, Stud. Mycol. 49: 28. 2004.
Penicillium nordicum Dragoni & Cantoni ex Ramírez, Adv. Pen. Asp. Syst.: 139. 1985.
Penicillium osmophilum Stolk & Veenbaas-Rijks, Ant. van Leeuwenhoek 40: 1. 1974.
Penicillium palitans Westling, Ark. Bot. 11: 83. 1911.
Penicillium polonicum Zaleski, Bull. Int. Acad. Pol. Sci. Lett., Sér. B 1927: 445. 1927.
Penicillium radicicola Overy & Frisvad, Syst. Appl. Microbiol.: 633. 2003.
Penicillium solitum Westling, Ark. Bot. 11: 65. 1911.
Penicillium thymicola Frisvad & Samson, Stud. Mycol. 49: 29. 2004.
Penicillium tricolor Frisvad, Seifert, Samson & Mills, Can. J. Bot. 72: 937. 1994.
Penicillium tulipae Overy & Frisvad, Syst. Appl. Microbiol. 634. 2003.
Penicillium venetum (Frisvad) Frisvad, Int. Mod. Tax. Meth. Pen. Asp. Clas.: 275. 2000.
Penicillium verrucosum Dierckx, Ann. Soc. Scient. Brux. 25: 88. 1901.
Penicillium viridicatum Westling, Ark. Bot. 11: 88. 1911.
Clade 16: Section Digitata (as “Digitatum”) Frisvad & Samson, Stud. Mycol. 49: 26. 2004.
In: Penicillium subgenus Penicillium
Type: Penicillium digitatum (Pers.:Fr.) Sacc.
Section Digitata is represented by one species, P. digitatum. This species is unique in its combination of features. Conidiophore and conidial structures are irregular and exceptionally large for Penicillium, usually biverticillate rather than terverticillate and the conidia are olive-green. The conidia are large and ellipsoidal to cylindrical (Frisvad & Samson 2004). Partial β-tubulin (Samson et al. 2004) and RPB2 data (Fig. 13) shows that this section is situated in subgenus Penicillium. Frisvad & Samson (2004) is followed here and this section is retained for P. digitatum.
Penicillium digitatum (Pers.:Fr.) Sacc., Fung. Ital.: 894. 1881.
Clade 17: Section Penicillium
= Bulliardium Biourge, La Cellule 33: 107. 1923 (= Asymetrica).
In: Penicillium subgenus Penicillium
Type: Penicillium expansum Link
Frisvad & Samson (2004) are followed here in their delimitation of section Penicillium. The recently described species P. brevistipitatum is added to this list, because it is closely related to P. coprophilum (Fig. 13). The analysis of our partial RPB2 data (Fig. 13) indicate sthat this section is polyphyletic. In contrast, partial β-tubulin data (Samson et al. 2004) showed that members of this section are on a single branch with 100 % bootstrap support. Frisvad & Samson (2004) are followed and the following species are accommodated in section Penicillium:
Penicillium brevistipitatum Wang & Zhuang, Mycotaxon 93: 234. 2005.
Penicillium clavigerum Demelius, Verh. Zool.-Bot. Ges. Wien 72: 74. 1922.
Penicillium concentricum Samson, Stolk & Hadlok, Stud. Mycol. 11: 17. 1976.
Penicillium coprobium Frisvad, Mycologia 81: 853. 1989.
Penicillium coprophilum (Berk. & Curt.) Seifert & Samson, Adv.Pen. Asp. Syst.: 145. 1985.
Penicillium dipodomyicola (Frisvad, Filt. & Wicklow) Frisvad, Int. Mod. Meth. Pen. Asp. Clas.: 275. 2000.
Penicillium expansum Link, Ges. Naturf. Freunde Berlin Mag. Neuesten Entdeck. Gesammten Naturk. 3: 16. 1809.
Penicillium formosanum Hsieh, Su & Tzean, Trans. Mycol. Soc. R.O.C. 2: 159. 1987.
Penicillium gladioli McCulloch & Thom, Science, N.Y. 67: 217. 1928.
Penicillium glandicola (Oud.) Seifert & Samson, Adv. Pen. Asp. Syst.: 147. 1985.
Penicillium griseofulvum Dierckx, Ann. Soc. Scient. Brux. 25: 88. 1901.
Penicillium italicum Wehmer, Hedwigia 33: 211. 1894.
Penicillium marinum Frisvad & Samson, Stud. Mycol. 49: 20. 2004.
Penicillium sclerotigenum Yamamoto, Scient. Rep. Hyogo Univ. Agric., Agric. Biol. Ser. 2, 1: 69. 1955.
Penicillium ulaiense Hsieh, Su & Tzean, Trans. Mycol. Soc. R.O.C. 2: 161. 1987.
Penicillium vulpinum (Cooke & Massee) Seifert & Samson, Adv. Pen. Asp. Syst.: 144. 1985.
Clade 18: section Roquefortorum (as “Roqueforti”) Frisvad & Samson, Stud. Mycol. 49: 16. 2004.
In: Penicillium subgenus Penicillium
Type: Penicillium roqueforti Thom
Frisvad & Samson (2004) erected section Roqueforti for rapidly growing species forming strictly velutinous colonies. All species form terverticillate rough walled conidiophores and are able to grow at low pH values (e.g. on media containing 0.5 % acetic acid), at high alcohol concentrations and at elevated CO2 levels. Members of this section appear to have a symbiotic relationship with lactic acid bacteria and certain acid-tolerant yeasts. Currently, four species are described in this section (Frisvad & Samson 2004, Houbraken et al. 2010a):
Penicillium carneum (Frisvad) Frisvad, Microbiology, UK, 142: 546. 1996.
Penicillium paneum Frisvad, Microbiology (UK) 142: 546. 1996.
Penicillium psychrosexualis Houbraken & Samson, IMA Fungus 1:174. 2010.
Penicillium roqueforti Thom, Bull. Bur. Anim. Ind. US Dept. Agric. 82: 35, 1906.
Clade 19: section Chrysogena Frisvad & Samson, Stud. Mycol. 49: 17. 2004.
In: Penicillium subgenus Penicillium
Type: Penicillium chrysogenum Thom
Members of the section Chrysogena are characterised by the formation of ter- and/or quarterverticillate, smooth walled conidiophores with relatively small phialides. Colonies have a velvety texture and species are tolerant to salt and the majority is capable to produce penicillin (Frisvad & Samson 2004). Four teleomorph species belong to section Chrysogena: P. sinaicum, P. egyptiacum, P. molle and P. kewense (Fig. 13). Penicillium egyptiacum was described as a holomorphic species (van Beyma 1933). Pitt (1980) transferred the teleomorphic state to Eupenicillium (E. egyptiacum) and introduced a new name for the Penicillium morph (P. nilense). This name is not used here and P. egyptiacum is re-instated. There are several taxonomic problems concerning P. kewense. Brefeld (1874) was the first who described the formation of a teleomorph in Penicillium. He identified the studied species as “Penicillium crustaceum Fries, Penicillium glaucum Link”. It is, however, very questionable whether the strains studied by Brefeld truly represented the species described by Link and Fries (Stolk & Scott 1967). Stolk & Scott (1967) are followed here; they agreed that the fungus described by Smith (1961b) as Penicillium kewense resembles Brefeld's fungus. Based on the data of Samson et al. (2004), Houbraken et al. (2011a) and Fig. 13, the following species are accommodated in section Chrysogena.
Penicillium aethiopicum Frisvad, Mycologia 81: 848. 1990.
Penicillium chrysogenum Thom, Bull. Bur. Anim. Ind. U.S. Dep. Agric. 118: 58. 1910.
Penicillium confertum (Frisvad et al.) Frisvad, Mycologia 81: 852. 1990.
Penicillium dipodomyis (Frisvad, Filtenborg & Wicklow) Banke, Frisvad & Rosendahl, Int. Mod. Meth. Pen. Asp. Clas., 270. 2000.
Penicillium egyptiacum van Beyma, Zentralbl. Bakteriol., 2. Abt., 88: 137. 1933. (syn. P. nilense).
Penicillium flavigenum Frisvad & Samson, Mycol. Res. 101: 620. 1997.
Penicillium kewense Smith, Trans. Br. Mycol. Soc. 44: 42. 1961 (syn. E. crustaceum).
Penicillium molle Pitt, The Genus Penicillium: 148, 1980 [“1979”].
Penicillium mononematosum (Frisvad et al.) Frisvad, Mycologia 81:857. 1990.
Penicillium nalgiovense Laxa, Zentralbl. Bakteriol., 2. Abt., 86: 160. 1932.
Penicillium persicinum Wang, Zhou, Frisvad & Samson, Ant. van Leeuwenhoek 86: 177. 2004.
Penicillium rubens Biourge, Cellule 33: 265. 1923.
Penicillium sinaicum Udagawa & Ueda, Mycotaxon 14: 266. 1982.
Clade 20: section Turbata Houbraken & Samson, sect. nov. MycoBank MB563133.
Sectio in Penicillio subgen. Penicillo. Conidiophoris delicatis et symmetricis, biverticillatis; formatione acoris extroliti penicillici.
In: Penicillium subgenus Penicillium
Type: Penicillium turbatum Westling
Section Turbata is phylogenetically closely related to section Paradoxa, and P. matriti, P. bovifimosum and P. turbatum are accommodated in this section. These species form rather delicate and symmetric biverticillate Penicillium conidiophores. Furthermore, penicillic acid is produced by all these species, and P. bovifimosum, P. turbatum and selected strains of P. matriti produce a fumagillin-like compound (Tuthill & Frisvad 2002).
Penicillium bovifimosum (Tuthill & Frisvad) Houbraken & Samson, Stud. Mycol. 70: 47. 2011 (this study).
Penicillium matriti Smith, Trans. Br. Mycol. Soc. 44: 44. 1961.
Penicillium turbatum Westling, Ark. Bot. 11: 128. 1911 (syn. E. baarnense, P. baarnense, this study).
Clade 21: section Paradoxa Houbraken & Samson, sect. nov. MycoBank MB563134.
Sectio in Penicillio subgen. Penicillo. Speciebus saepe cum conidiophoris typi Aspergillus et odore molesti efferenti.
In: Penicillium subgenus Penicillium
Type: Aspergillus paradoxus Fennell & Raper
Aspergillus paradoxus, A. malodoratus, A. crystallinus and P. atramentosum form a well-supported clade (85 % bs, 1.00 pp). Phylogenetic and extrolite analysis shows that the first three species belong in Penicillium and will be transferred to this genus (R.A. Samson, unpubl. data). Besides a similar type of Aspergillus anamorph, these three species also produce a strong, unpleasant smell. Penicillium atramentosum is phylogenetically basal to these three species. This species is alkaliphilic and unpublished results show that this character is shared with A. paradoxus. More research is needed to determine whether A. malodoratus and A. crystallinus also share this feature.
Penicillium atramentosum Thom, Bull. Bur. Anim. Ind. US Dept. Agric. 118: 65. 1910.
Aspergillus crystallinus Kwon-Chung & Fennell, The Genus Aspergillus: 471. 1965.
Aspergillus malodoratus (Kwon-Chung & Fennell), The Genus Aspergillus: 468. 1965.
Aspergillus paradoxus Fennell & Raper, Mycologia 47: 69.
Clade 22: section Brevicompacta Thom, The Penicillia: 289. 1930.
= section Coronata Pitt, The Genus Penicillium: 392, 1980.
In: Penicillium subgenus Penicillium
Type: Penicillium brevicompactum Dierckx
Members of the section Brevicompacta are characterised by conidiophores with long and broad stipes. The conidial heads look superficially like Aspergillus heads in the stereomicroscope. Section Coronata, typified with P. olsonii, is placed here in synonymy. Recently, P. neocrassum and P. astrolobatum were described in this section (Serra & Peterson 2007) and partial RPB2 data (Fig. 13) show that also P. tularense and P. fennelliae belong here. The production of the extrolites asperphenamate and the unknown metabolite O (Frisvad & Samson 2004) is shared by P. olsonii, P. brevicompactum and P. bialowiezense. More research in needed to determine whether these metabolites are also produced by the other members of section Brevicompacta. Based on literature (Frisvad & Samson 2004, Peterson 2004, Serra & Peterson 2007) and partial RPB2 data (Fig. 13) the following species are accommodated in section Brevicompacta:
Penicillium astrolobatum Serra & Peterson, Mycologia 99: 80. 2007.
Penicillium bialowiezense Zaleski, Bull. Int. Acad. Pol. Sci. Lett., Sér. B, 1927: 462. 1927 (syn. P. biourgeianum).
Penicillium brevicompactum Dierckx, Ann. Soc. Scient. Brux. 25: 88. 1901.
Penicillium fennelliae Stolk, Ant. van Leeuwenhoek 35: 261. 1969.
Penicillium neocrassum Serra & Peterson, Mycologia 99: 81. 2007.
Penicillium olsonii Bainier & Sartory, Ann. Mycol. 10: 398. 1912.
Penicillium tularense Paden, Mycopathol. Mycol. Appl. 43: 264. 1971.
Clade 23: section Ramosa (as “Ramosum”) Stolk & Samson, Adv. Pen. Asp. Syst.: 179. 1985.
In: Penicillium subgenus Penicillium
Type: Penicillium lanosum Westling
Figure 13 shows that section Ramosa is not well resolved and members of this section are on a well-supported branch with section Brevicompacta members (100 % bs, 1.00 pp). We split this clade in two sections based on phenotypic characters and extrolite patterns. Members of the section Lanosa form biverticillate or terverticillate conidiophores with divergent rami (twice biverticillate), while members of sect. Brevicompacta have appressed branches. Penicillium jamesonlandense, P. lanosum, P. ribeum, P. raistrickii, P. soppii and P. swiecickii produce different combinations of cycloaspeptide, kojic acid and griseofulvin (Frisvad & Filtenborg 1990, Frisvad et al. 2006) and these extrolites are not been found in section Brevicompacta (Frisvad & Samson 2004). More research is needed to determine if the other members of this section also produce cycloaspeptide, kojic acid and/or griseofulvin.
Penicillium scabrosum is basal to the members of sections Brevicompacta and Ramosa. This species is tentatively accommodated in sect. Ramosa based on the formation of divaricate branches (Frisvad et al. 1990a). In contrast, cyclopenin, cyclopenol, viridicatin, penigequinolone A and B and fumagillin are produced by P. scabrosum and these extrolites are not detected in species belonging to sect. Ramosa (Frisvad et al. 1990a, Larsen et al. 1999). In the original description of P. virgatum, a relationship with P. daleae was suggested (Kwasna & Nirenberg 2005). However, these two species are unrelated and our partial RPB2 data suggest P. virgatum is related to members of section Ramosa (Fig. 13). Based on data presented in Fig. 13 and in Frisvad et al. (2006), the following species are placed in section Ramosa:
Penicillium jamesonlandense Frisvad & Overy, Int. J. Syst. Evol. Microbiol. 56: 1435. 2006.
Penicillium kojigenum Smith, Trans. Br. Mycol. Soc. 44: 43. 1961.
Penicillium lanosum Westling, Ark. Bot. 11: 97. 1911.
Penicillium raistrickii Smith, Trans. Br. Mycol. Soc.18: 90. 1933.
Penicillium ribeum Frisvad & Overy, Int. J. Syst. Evol. Microbiol. 56: 1436. 2006.
Penicillium sajarovii Quintanilla, Avances Nutr. Mejora Anim. Aliment. 22: 539. 1981.
Penicillium scabrosum Frisvad, Samson & Stolk, Persoonia 14: 177. 1990.
Penicillium simile Davolos, Pietrangeli, Persiani & Maggi, J. Syst. Evol. Microbiol., in press.
Penicillium soppii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 476. 1927.
Penicillium swiecickii Zaleski, Bull. Int. Acad. Pol. Sci. Lett., Sér. B 1927: 474. 1927.
Penicillium virgatum Nirenberg & Kwasna, Mycol. Res. 109: 977. 2005.
Clade 24: section Canescentia Houbraken & Samson, sect. nov. MycoBank MB563135.
Sectio in Penicillio subgen. Penicillo. Structuris symmetricis biverticillatis, raro cum ramulis pluribus. Phialidibus simplicibus, brevibus (7–9 μm), cum collo brevi, interdum distincte attenuato.
In: Penicillium subgenus Penicillium
Type: Penicillium canescens Sopp
Members of section Canescentia are soil-borne and are characterised by the formation of symmetrical biverticillate structures with infrequently an additional branch. Phialides are simple and short (7–9 μm) with a broadly cylindrical to slightly or more definitely swollen base and a short, occasionally more pronounced narrowed neck. This section has not been a subjected to a thorough phylogenetic study and unpublished sequence results show that several synonyms should be raised to species level. Partial RPB2 data (Fig. 13) shows that following species are placed in section Canescentia.
Penicillium canescens Sopp, Skr. Vidensk.-Selsk. Christiana, Math.-Naturvidensk. Kl. 11: 181. 1912.
Penicillium jensenii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 494. 1927.
Penicillium yarmokense Baghdadi, Nov. Sist. Niz. Rast. 5: 99. 1968.
Penicillium janczewskii Zaleski, Bull. Int. Acad. Polon. Sci., Cl. Sci. Math., Sér. B, Sci. Nat., 1927: 488. 1927.
Penicillium antarcticum Hocking & McRae, Polar Biology 21: 103. 1999.
Penicillium atrovenetum Smith, Trans. Br. Mycol. Soc. 39: 112. 1956.
Penicillium novae-zeelandiae van Beyma, Ant. van Leeuwenhoek 6: 275. 1940.
Penicillium coralligerum Nicot & Pionnat, Bull. Soc. Mycol. France 78: 245. 1963 [“1962”].
Clade 25: section Eladia (Smith) Stolk & Samson, Adv. Pen. Asp. Syst.: 169. 1985.
In: Penicillium subgenus Penicillium
Type: Penicillium sacculum Dale
The genus Eladia is synonymised with Penicillium and two species are placed here in section Eladia: P. sacculum and P. senticosum (Fig. 7, clade 25 and Fig. 13). Penicillium sacculum and P. senticosum grow rather well on MEA (and poorly on Czapek agar) and their colonies on MEA are velvety and dull-green, brownish-green or olive-brown coloured. Phialides are born irregularly on the stipes, subterminally as well as terminally, short, 4–7 μm, with a swollen base, and at the apex tapering abruptly into a short narrow neck. Conidia are distinctly ornamented (Smith 1961b, Pitt 1980, Stolk & Samson 1983, Stolk & Samson 1985). No type material could be obtained from Eladia pachyphialis and Eladia tibetensis and their taxonomic position remains uncertain. Based on their protologues, it is likely that these species belong to Penicillium.
Penicillium sacculum Dale apud Biourge, Cellule 33: 323. 1923.
Penicillium senticosum Scott, Mycopathol. Mycol. Appl. 36: 5. 1968.
Excluded and unclassified Penicillia
Over 250 Penicillium and Eupenicillium species are mentioned in the list of accepted Penicillium species (Pitt et al. 2000) and a fair amount of these do not belong to Penicillium s. str. The majority of these excluded species are currently classified in Talaromyces and an overview of species is given by Samson et al. (2011). Only a small number of species do not belong to either genus. These include P. arenicola, P. inflatum, P. kabunicum, P. lineatum, P. megasporum and P. moldavicum. Figure 1 shows that P. arenicola is closely related to Phialomyces (clade 6) and P. megasporum belongs to the clade 3 (Hamigera/Warcupiella). Both species should be transferred to other genera. Unpublished data (R.A. Samson) shows that P. inflatum belongs to Aspergillus and this species will be combined in that genus. Penicillium kabunicum and P. moldavicum are phylogenetically related and were included in the initial analyses of Trichocomaceae. Both species were together on a single branch and did not fit with any members of this family (J. Houbraken, unpubl. data). These two species belong to another (related) family and might represent a new genus. Penicillium lineatum was described as the anamorph of Hamigera striata (Pitt 1980). Hamigera striata is accommodated in clade 3 (Fig. 1) and does therefore not belong to Penicillium s. str. Penicillium syriacum was included in the list of accepted names (Pitt et al. 2000), but the illustration and description of P. syriacum by Baghdadi (1968) and examination of ex-type material from ATCC, CBS and IMI indicated a mixed culture. This species is considered a nomen ambiguum (Christensen et al. 1999).
The phylogenetic position of P. resedanum needs further attention. Pitt (1980) and Ramírez (1982) placed P. resedanum in section Aspergilloides based on the formation of monoverticillate conidiophores. Pitt (1980) already noted that this species form acerose phialides with weak growth on G25N, suggesting a relationship with Talaromyces (and subgenus Biverticillium). A BLAST search on GenBank with ITS sequences of NRRL 578T (AF033398) indicates a relationship with Talaromyces.
Penicillium griseolum is listed as a synonym of P. restrictum (Pitt et al. 2000). However, Fig. 7 shows that these species are phylogenetically unrelated. In our study, we did not find any species closely related to P. griseolum and this species might represent a separate section. We have chosen not to proceed with the description of this new section for this species until additional related species are described.
Penicillium arenicola Chalabuda, Bot. Mater. Otd. Sporov. Rast. 6: 162. 1950 (= clade 6, related to Phialomyces).
Penicillium inflatum Stolk & Malla, Persoonia 6: 197. 1971. (= Aspergillus inflatus, R.A. Samson, unpubl. data).
Penicillium kabunicum Baghdadi, Novosti Sist. Nizs. Rast.: 98. 1968 (unrelated to Penicillium, J. Houbraken, unpubl. data).
Penicillium lineatum Pitt, The Genus Penicillium: 485. 1980 [“1979”] (= Hamigera striata).
Penicillium megasporum Orpurt & Fennell, Mycologia 47: 233. 1955 (= clade 3, related to Hamigera and Warcupiella).
Penicillium moldavicum Milko & Beliakova, Novosti Sist. Nizs. Rast. 1967: 255. 1967 (unrelated to Penicillium, J. Houbraken, unpubl. data).
Penicillium syriacum Baghdadi, Novosti Sist. Nizs. Rast. 1968: 111. 1968 (nomen ambiguum, Christensen et al. 1999).
Character analysis
The classification proposed in the monographs of Raper & Thom (1949), Pitt (1980) and Ramírez (1982) is not concordant with the new classification system proposed here. One of the most important characters in these monographs is the branching pattern of the Penicillium conidiophore. Our study shows that monoverticillate (Aspergilloid) conidiophores occur in various sections (e.g. clades 1, 2, 6, 8, 10, 12, 25). Sections Aspergilloides (clade 1) and Eladia (clade 25) comprise only strictly monoverticillate species, while mono- and biverticillate species are intermingled in the other clades. The occurrence of both structures in multiple phylogenetic clades (sections) indicates that reduction of the Penicillium conidiophore might have occurred various times. Most of the species belonging to section Citrina (clade 14) are symmetrically biverticillate and occasionally additional branches with the same branching pattern as the main axis (“double symmetrically biverticillate”) occurs. Species belonging to section Lanata-divaricata are mainly divaricate and the metulae are borne terminally, subterminally and in intercalary positions. Terverticillate conidiophores mainly occur in clades 15–18 and section Chrysogena (clade 19) comprises species with quarterverticillate condiophores. The monoverticillate species Penicillium sacculum and P. senticosum belong to clade 25. This clade is positioned in subgenus Penicillium and has therefore a unique branching pattern for this subgenus. Growth rates on agar media are also frequently used for classification. Some sections mainly comprise fast growing species (e.g. clades 1, 2, 11, 16, 18, 19, 25) while in other clades slow growing species predominate (e.g. clades 3, 6, 8, 9). The new proposed sectional classification will serve as a starting point to investigate phenotypic characters used for classification.
TAXONOMIC IMPLICATIONS
Penicillium asymmetricum (Subramanian & Sudha) Houbraken & Samson, comb. nov. MycoBank MB561963.
Basionym: Thysanophora asymmetrica Subramanian & Sudha, Kavaka 12: 88. 1985.
Penicillium bovifimosum (Tuthill & Frisvad) Houbraken & Samson, comb. nov. MycoBank MB561957.
Basionym: Eupenicillium bovifimosum Tuthill & Frisvad, Mycologia 94: 241. 2002.
Penicillium coniferophilum Houbraken & Samson, nom. nov. MycoBank MB561968.
Basionym: Thysanophora striatispora Barron & Cooke, Mycopathologia et Mycologia Applicata 40: 353. 1970, non Penicillium striatisporum Stolk, Ant. van Leeuwenhoek 35: 268. 1969.
Note: The name P. striatisporum is already occupied and therefore a new name is proposed.
Penicillium glaucoalbidum (Desmazières) Houbraken & Samson, comb. nov. MycoBank MB561965.
Basionym: Sclerotium glaucoalbidum Desmazières, Annales des Sciences Naturelles, Botanique 16: 329. 1851.
= Thysanophora glaucoalbida (Desm.) Morelet, Annales de la Société des Sciences Naturelles et Archéologie de Toulon et Var 20: 104. 1968.
= Thysanophora penicillioides (Roumeguère) Kendrick, Can. J. Bot. 39: 820. 1961.
Note: Virtually all of the published information relating to P. glaucoalbidum has used the binomial Thys. penicillioides. Iwamoto et al. (2005) aggregated sequence data of seven European and North American P. glaucoalbidum (as Thys. penicillioides) strains with Japanese strains. The strains formed nine lineages and according to phylogenetic species recognition by the concordance of genealogies, respective lineages correspond to phylogenetic species.
Penicillium hennebertii Houbraken & Samson, nom. nov. MycoBank MB561964.
Basionym: Thysanophora canadensis Stolk & Hennebert, Persoonia 5: 189. 1968, non Penicillium canadense Smith, Trans. Br. mycol. Soc. 39: 113. 1956.
Note: A new name was sought for this species, as the species name “canadensis” is already occupied.
Penicillium laeve (K. Ando & Manoch) Houbraken & Samson, comb. nov. MycoBank MB561960.
Basionym: Torulomyces laevis K. Ando & Manoch, Mycoscience 39: 317. 1998.
Penicillium longisporum (Kendrick) Houbraken & Samson, comb. nov. MycoBank MB561966.
Basionym: Thysanophora longispora Kendrick, Can. J. Bot. 39: 826. 1961.
Penicillium malachiteum (Yaguchi & Udagawa) Houbraken & Samson, comb. nov. MycoBank MB561971.
Basionym: Chromocleista malachitea Yaguchi & Udagawa, Trans. Mycol. Soc. Japan 34: 102. 1993.
= Geosmithia malachitea Yaguchi & Udagawa, Trans. Mycol. Soc. Japan 34: 102. 1993.
Penicillium melanostipe Houbraken & Samson, nom. nov. MycoBank MB561970.
Basionym: Thysanophora verrucosa Mercado, Gené & Guarro, Mycotaxon 67: 419. 1998, non Penicillium verrucosum Dierckx, Annales de la Société Scientifique de Bruxelles 25: 88. 1901.
Note: The name Penicillium verrucosus is already occupied and therefore the name melanostipe, which is referring to the pigmented stipe of this species, is proposed.
Penicillium ovatum (K. Ando & Nawawi) Houbraken & Samson, comb. nov. MycoBank MB561961.
Basionym: Torulomyces ovatus K. Ando & Nawawi, Mycoscience 39: 317. 1998.
Penicillium parviverrucosum (K. Ando & Pitt) Houbraken & Samson, comb. nov. MycoBank MB561962.
Basionym: Torulomyces parviverrucosus K. Ando & Pitt, Mycoscience 39: 317. 1998.
Penicillium porphyreum Houbraken & Samson, nom. nov. MycoBank MB561959.
Basionym: Monocillium humicola Barron var. brunneum M. Christensen & Backus, Mycologia 56: 498. 1964, non Penicillium brunneum Udagawa, J. agric. Sci. Tokyo Nogyo Daigaku 5: 16. 1959.
= Torulomyces brunneus (M. Christensen & Backus) K. Ando, Mycoscience 39: 314. 1998.
Note: The name Penicillium brunneum is already occupied (Udagawa et al. 1959) and therefore the name P. porphyreum is proposed. The epithet porphyreum refers to the red-brown reverse of this species.
Penicillium saturniforme (Wang & Zhuang) Houbraken & Samson, comb. nov. MycoBank MB561958.
Basionym: Eupenicillium saturniforme Wang & Zhuang, Mycopathologia 167: 300. 2009.
Penicillium taiwanense (Matsushima) Houbraken & Samson, comb. nov. MycoBank MB561969.
Basionym: Phialomyces taiwanensis Matsushima, Matsushima Mycological Memoirs 4: 12. 1985.
= Thysanophora taiwanensis (Matsush.) Mercado, Gené & Guarro, Mycotaxon 67: 421. 1998.
Note: This species was originally described as Phialomyces taiwanensis. Based on micro-morphological features, Mercado-Sierra et al. (1998) transferred this species to Thysanophora taiwanensis.
Supplemental Information
Table S1.
Penicillium strains used in the study of the infrageneric classification (addition to those mentioned in Table 1).
Acknowledgments
Neriman Yilmaz and Barbara Favie are thanked for testing various primer pairs and generating sequences. Uwe Braun is thanked for providing the Latin diagnosis and advice on nomenclature issues. Jens Frisvad is acknowledged for providing various isolates and the reviewers for their useful suggestions. Marjan Vermaas is thanked for preparing the photographic plates.
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Wikipedia (Showing 9 of 9)
- https://en.wikipedia.org/wiki/Penicillium_glaucoalbidum
- https://en.wikipedia.org/wiki/Penicillium_humicoloides
- https://en.wikipedia.org/wiki/Penicillium_lineatum
- https://en.wikipedia.org/wiki/Penicillium_osmophilum
- https://en.wikipedia.org/wiki/Penicillium_corynephorum
- https://en.wikipedia.org/wiki/Penicillium_saturniforme
- https://en.wikipedia.org/wiki/Trichocomaceae
- https://en.wikipedia.org/wiki/Penicillium_javanicum
- https://en.wikipedia.org/wiki/Penicillium_parviverrucosum
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