Abstract
Free full text
First Records of Rare Ascomycete Fungi, Acrostalagmus luteoalbus, Bartalinia robillardoides, and Collariella carteri from Freshwater Samples in Korea
Abstract
The distribution and occurrence of rare ascomycete fungi within freshwater samples in Korea was investigated. Three rare fungal strains, CNUFC-YR537-1, CNUFC-CNUP1-1, and CNUFC-NDR3-1, were isolated using serial dilution method. On the basis of their morphological characteristics and phylogenetic analysis of their internal transcribed spacer regions and 28S rDNA sequences, the three isolates were identified as Acrostalagmus luteoalbus, Bartalinia robillardoides, and Collariella carteri, respectively. To our knowledge, these are the first records of rare genera Acrostalagmus, Bartalinia, and Collariella from Korea, and the first reports of A. luteoalbus, B. robillardoides, and C. carteri from freshwater samples.
1. Introduction
Freshwater fungi have an important role in the decomposition of organic matter in ecological systems, by virtue of producing enzymes that break down wood and producing bioactive compounds against pathogenic bacteria, fungi, and nematodes [1–4]. There are more than 622 species (170 genera) of Ascomycetes; more than 226 species of Hyphomycetes (55 genera); and 183 species of Trichomycetes (3 orders), while little is known about the Basidiomycetes and Zygomycetes [3].
Sordariomycetes is one of the largest classes of Ascomycetes, with six subclasses, 32 orders, 105 families, and 1331 genera [5]. Its species are characterized by nonlichenized, flask-shaped fruiting bodies (perithecia) and unitunicate asci [6]. They can be found in soil, dung, leaf litter, fresh water, plants, arthropods, and mammals [3,5,7,8].
The genus Acrostalagmus, which belongs to the class Sordariomycetes, order Hypocreales, and family Hypocreaceae, was established by Corda (1838) [9], with the type species A. cinnabarinus Corda. The species belonging to this genus are characterized as verticillate conidiophores, with hyaline, egg-shaped conidia formed singly [10]. Members of Acrostalagmus are found in saffron soil, needle mushroom, vermicompost, and branches of cacao [11–14]. They are also known for their ability to produce a variety of secondary metabolites. To date, 27 species belonging to this genus are known, according to the Index Fungorum (www.indexfungorum.org).
The genus Bartalinia, which belongs to the class Sordariomycetes, order Amphisphaeriales, and family Bartaliniaceae, was established by Tassi (1900) [15], with the type species Bartalinia robillardoides. It is characterized by the production of fusiform conidia with an acute or blunt apex and having three to four septate. Members of the genus have frequently been isolated from the leaves, stems of medicinal plants, or dead aerial spines of Rosa canina L. [16–19]. B. robillardoides has been reported to produce taxol, an anticancer drug [20]. Several types of compounds have been investigated from B. robillardoides strain LF550, such as three new chloroazaphilones named helicusin E, isochromophilone X, and isochromophilone XI, which expressed antimicrobial activity towards Bacillus subtilis, Staphylococcus lentus, Candida albicans, Trichophyton rubrum, and Septoria tritici, and also inhibited PDE4 and AChE [21]. Currently, there are 17 accepted species in this genus [22].
The genus Collariella, which belongs to the class Sordariomycetes, order Sordariales, and family Chaetomiaceae, was introduced by Wang et al. [23]. Based on phylogenies derived from ITS, LSU rDNA, rpb2, and tub2 sequence data combined with morphological observations, seven species have been recognized [23]. Currently, nine species have been registered in Index Fungorum. The species belonging to this genus are characterized by the production of a dark collar-like apex around the ostiolar pore of the ascomata [23]. They are found in soil, dust, and air [23–25]. Some of them have been reported to produce a variety of metabolites, including chaetoquadrin E, cochliodinol B, prenisatin, and SB236049/SB236050/SB238569 [23].
In Korea, many studies on the fungal diversity of various habitats have been conducted, although the occurrence of freshwater fungi remains poorly understood. Until now, only five new species and eight new records from freshwater habitat have been reported in Korea [19,26–30].
During our collection from freshwater samples, three rare species were found in Korea: A. luteoalbus, B. robillardoides, and C. carteri.
2. Materials and methods
2.1. Isolation of fungal strains from freshwater samples
Freshwater samples were collected from a branch stream of the Nakdong river located in Gyeongsangbuk-do, the Yeongsan river located in Gwangju, and a pond located in the Chonnam National University Arboretum, Gwangju, Korea. The samples were transported in sterile 50-mL Falcon tubes and stored at 4°C until examination. Serial dilution methods were employed using potato dextrose agar (PDA), malt extract agar (MEA), and corn meal agar (CMA). The media and method used were based on the protocol described by Wanasinghe et al. [19] and Nguyen et al. [31]. The plates were incubated at 25°C for 3–7days. To isolate pure cultures, individual colonies with various morphologies were picked up, transferred to PDA, and subcultured until pure mycelia were obtained. All pure isolates, including those of A. luteoalbus, B. robillardoides, and C. carteri, were stored in 20% glycerol at −80°C at the Chonnam National University Fungal Collection (CNUFC), Gwangju, Korea. A. luteoalbus, B. robillardoides, and C. carteri strains isolated in our study were designated CNUFC-YR537-1 and CNUFC-YR537-2, CNUFC-CNUP1-1 and CNUFC-CNUP1-2, CNUFC-NDR3-1 and CNUFC-NDR3-2, respectively. Strains CNUFC-YR537-1, CNUFC-CNUP1-1, and CNUFC-NDR3-1 were also deposited at the Culture Collection of the Nakdonggang National Institute of Biological Resources (NNIBR, Sangju, Korea).
2.2. Morphological studies
For detailed morphological studies, CNUFC-YR537-1, CNUFC-CNUP1-1, and CNUFC-NDR3-1 strains were cultured on PDA, MEA, and CMA. The plates were incubated at 25°C in the dark for 7d. Samples were mounted in lactophenol solution (Junsei Chemical Co. Ltd., Tokyo, Japan) and observed under an Olympus BX51 microscope with DIC optics (Olympus, Tokyo, Japan). For scanning electron microscopy (SEM), samples were prepared as described previously [32].
2.3. DNA extraction, polymerase chain reaction (PCR), and sequencing
Strains CNUFC-YR537-1, CNUFC-CNUP1-1, and CNUFC-NDR3-1 were grown on PDA, covered with cellophane at 25°C for 4–5days. Genomic DNA was extracted using the Solg TM Genomic DNA prep. Kit (Solgent Co. Ltd., Daejeon, South Korea). The internal transcribed spacers (ITS1, and ITS2) and 5.8S region of the ribosomal DNA were amplified with the primer pair ITS1 and ITS4 [33]. The large subunit of 28S rDNA was amplified with the primer pair LROR and LR5F [34]. The PCR amplification mixture (total volume, 20μL) was comprised of 2μl of the fungal DNA template (10ng), 1.5μl of each primer (5pM/μL), 1μl Accupower® PCR premix (Bioneer Corp., Daejeon, South Korea) containing Taq DNA polymerase, dNTPs, buffer, and tracking dye, and 14μl sterile water. The amplification parameters were as follows: an initial denaturation step at 95°C for 5min, followed by 35 thermal cycles with denaturation at 94°C for 30s, annealing at 55°C (ITS) or 52°C (28S) for 30s, and extension at 72°C for 1min, followed by a final extension at 72°C for 10min. The PCR products were purified using the Accuprep® PCR Purification Kit (Bioneer Corp.). DNA sequencing was performed in an ABI 3700 Automated DNA sequencer (Applied Biosystems Inc., Foster City, CA, USA).
2.4. Phylogenetic analysis
The fungal sequences obtained from the GenBank database (Table 1) were aligned using Clustal_X v.1.83 [35] and edited with Bioedit v.5.0.9.1 [36]. Phylogenetic trees based on the ITS rDNA and 28S sequences were constructed using the neighbor-joining method in MEGA 6 [37]. Colletotrichum boninense, Glomerella cingulate, Microascus trigonosporus, and Pestalotiopsis malayana were used as outgroups. The reliability of internal branches was assessed using the p-distance substitution model with 1000 bootstrap replications. Sequence data were compared with similar sequences available in the GenBank databases using BLASTn.
Table 1.
Taxon name | Collection no. (Isolate no.) | GenBank accession no. | |
---|---|---|---|
ITS | 28S | ||
Acremonium alcalophilum | CBS 114.92 | JX158421 | JX158443 |
Acrostalagmus annulatus | DAOM212126 | GU180632 | GU180646 |
Acrostalagmus luteoalbus | V209 | KJ443275 | KJ443145 |
Acrostalagmus luteoalbus | V208 | KJ443274 | KJ443144 |
Acrostalagmus luteoalbus | V207 | KJ443273 | |
Acrostalagmus luteoalbus | DO137 | KP050692 | |
Acrostalagmus luteoalbus | CBS 194.87 | EF543826 | |
Acrostalagmus luteoalbus | CNUFC-YR537-1 | MH482849 | MH482855 |
Acrostalagmus luteoalbus | CNUFC-YR537-2 | MH482850 | MH482856 |
Bartalinia robillardoides | CBS 122705 (T) | KJ710460 | KJ710438 |
Bartalinia robillardoides | CBS 122686 | EU552102 | |
Bartalinia robillardoides | CNUFC-CNUP1-1 | MH482847 | MH482853 |
Bartalinia robillardoides | CNUFC-CNUP1-2 | MH482848 | MH482854 |
Bartalinia rosicola | MFLUCC 17-0645 (T) | MG828872 | MG828988 |
Bartalinia laurina | HKUCC 6537 | AF405302 | AF382369 |
Bartalinia pondoensis | A1S1-D17 | KJ767127 | |
Bartalinia pondoensis | WSO118 | KU556132 | |
Bartalinia pondoensis | CLB55 | KU645988 | |
Bartalinia pondoensis | SQU-QU20 | KU945962 | |
Broomella rosae | MFLU 16-0244 | MG828990 | |
Broomella vitalbae | MFLUCC 14-1000 | KP757754 | |
Broomella vitalbae | MFLUCC 15-0023 | KP757751 | |
Collariella bostrychodes | CBS 586.83 | KX976642 | KX976739 |
Collariella bostrychodes | DTO 324-H3 | KX976644 | KX976740 |
Collariella bostrychodes | CBS 163.73 | KX976641 | KX976738 |
Collariella gracilis | CBS 249.75 | KX976649 | KX976744 |
Collariella gracilis | CBS 146.60 (T) | KX976648 | KX976743 |
Collariella carteri | CBS 128.85 (T) | KX976647 | KX976742 |
Collariella carteri | CNUFC-NDR3-1 | MH482845 | MH482851 |
Collariella carteri | CNUFC-NDR3-2 | MH482846 | MH482852 |
Collariella causiiformis | CBS 792.83 (T) | KX976646 | KX976741 |
Collariella quadrangulata | CBS 152.59 | KX976651 | KX976746 |
Collariella quadrangulata | CBS 142.58 | KX976650 | KX976745 |
Collariella robusta | CBS 551.83 | KX976652 | KX976747 |
Collariella robusta | CBS 508.84 | KX976653 | KX976748 |
Collariella virescens | CBS 148.68 (T) | KX976654 | KX976749 |
Collariella virescens | CBS 547.75 | KX976655 | KX976750 |
Colletotrichum boninense | 270 | FJ224116 | |
Dyrithiopsis lakefuxianensis | HKUCC 7303 | AF452047 | |
Glomerella cingulata | FAU 553 | AF543786 | |
Microascus trigonosporus | CBS 218.31 (T) | LM652443 | HG380436 |
Neotruncatella endophytica | EML-AS5-1 | KX216520 | KX216518 |
Neotruncatella endophytica | EML-AS5-2 | KX216521 | KX216519 |
Pestalotiopsis malayana | CBS 102220 | KM199306 | |
Phlogicylindrium uniforme | CBS 131312 | JQ044445 | |
Sodiomyces tronii | MAG1 | KJ443277 | KJ443147 |
Sodiomyces tronii | MAG3 | KJ443279 | KJ443149 |
Sodiomyces magadii | MAG2 | KJ443278 | KJ443148 |
Truncatella angustata | UCD2157OR | FJ794472 | |
Truncatella angustata | ICMP 7062 | AF382383 | |
Truncatella hartigii | CBS 118145 | DQ278912 | DQ278927 |
Truncatella helichrysi | CBS 123029 | EU552163 | |
Hyalotiella spartii | MFLUCC 15-0024 | KP757753 | |
Truncatella restionacearum | CBS 118150 | DQ278914 | |
Truncatella restionacearum | CMW 18755 | DQ278929 | |
Verticillium albo-atrum | CBS 130.51 | DQ825977 | |
Verticillium dahliae | 76 Greece | AF104926 | |
Verticillium dahliae | ATCC 16535 | AY489737 | |
Verticillium zaregamsianum | V204 | KJ443270 | KJ443140 |
Verticillium zaregamsianum | V203 | KJ443269 | KJ443139 |
Verticillium zaregamsianum | V202 | KJ443268 | KJ443138 |
Zetiasplozna acaciae | CPC 23421 | KJ869149 | KJ869206 |
Bold letters indicate isolates and accession numbers determined in our study.
ATCC: American Type Culture Collection, Manassas, VA, USA; CBS: Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands; CNUFC: Chonnam National University Fungal Collection, Gwangju, South Korea; CPC: Culture collection of Pedro Crous, housed at CBS; DAOM: Canadian Collection of Fungal Cultures, Ottawa, Canada; EML: Environmental Microbiology Laboratory Fungarium, Chonnam National University, Gwangju, South Korea; ITS: internal transcribed spacer; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Rai, Thailand; T: ex-type strain.
3. Results
3.1. Phylogenetic analysis
A BLAST search of ITS sequences via the NCBI database indicated that the isolates CNUFC-YR537-1, CNUFC-CNUP1-1, and CNUFC-NDR3-1 most closely resembled A. luteoalbus (GenBank accession no. KP050692), B. robillardoides (GenBank accession no. KJ710460), and C. carteri (GenBank accession no. KX976747), with 99.6% (542/544bp), 99.6% (539/541bp), and 99.8% (499/500bp) homology, respectively. The 28S sequences of A. luteoalbus (GenBank accession no. KJ443145), B. robillardoides (GenBank accession no. KJ710438), and C. carteri (GenBank accession no. KX976742) showed 100% (850/850bp), 99.8% (871/873bp), and 100% (487/487bp) homology with the 28S sequence of the isolates CNUFC-YR537-1, CNUFC-CNUP1-1, and CNUFC-NDR3-1, respectively.
On the basis of the ITS and 28S sequence analysis, the isolates CNUFC-YR537-1, CNUFC-CNUP1-1, and CNUFC-NDR3-1 were identical to A. luteoalbus, B. robillardoides, and C. carteri, respectively (Figures 1–3).
3.2. Taxonomy
3.2.1. Taxonomy of CNUFC-YR537-1
A. luteoalbus (Link) Zare, W. Gams & Schroers, Mycological Research 108 (5): 581 (2004) (Table 2, Figure 4).
Table 2.
Characteristics | Present isolate | A. luteoalbusa |
---|---|---|
Colony | Slow-growing, attaining a diameter of 24–26mm after 7 d, dull orange to orange-brown; reverse of colonies were orange, becoming light orange at the center | Slow-growing, attaining a diameter of 35–10mm after 10 d, dull orange to orange-brown |
Phialide | Flask-shaped, hyaline, measured 10–29×2.0–3.5 µm | Flask-shaped, hyaline, 12–23×2–4 µm |
Conidia | Conidia were oval, pale reddish, measured 3.5–6.2×2.2–2.9 µm | Conidia oval, pale reddish brown in mass, 3.5–5.0×2.0–2.5 µm |
aFrom the description by Zare et al. [10].
=Sporotrichum luteoalbum (Link), Magazin der Gesellschaft Naturforschenden Freunde Berlin 3 (1): 13 (1809).
=Verticillium luteoalbum (Link) Subram., Hyphomycetes: an account of Indian species, except Cercosporae: 649 (1971).
=Verticillium tenerum Nees, System der Pilze und Schwämme: 57, t. 4:55 (1817).
=Sporotrichum lateritium Ehrenb., Sylvae mycologicae Berolinenses: 22 (1818).
=Sporotrichum hippocastani Corda, Icones fungorum hucusque cognitorum 1: 10, t. 2:159 (1837).
=Acrostalagmus cinnabarinus Corda, Icones fungorum hucusque cognitorum 2: 15, t. 10:66 (1838).
=Sporotrichum luteoalbum Thüm., Fungi pomicoli. Monographische Beschreibung der auf den Obstfrüchten der gemässigten Klimate vorkommenden Pilze: 21 (1879).
=Sporotrichum vile P. Karst., Hedwigia 30: 303 (1891).
Description: Colonies of the strain grew slowly on PDA, appearing dull orange to orange-brown, and reaching 24–26mm in diameter after 7days of incubation at 25°C. The reverse of the colonies were orange, appearing a lighter orange in the centers. Conidiophores were erect, pale orange-brown, measured 33–121×2.0–4.0µm, and repeatedly verticillately branched in one to several orders. Phialides were flask-shaped, hyaline, and measured 10–29×2.0–3.5µm. Conidia were oval, pale reddish, and measured 3.5–6.2×2.2–2.9µm.
3.2.2. Taxonomy of CNUFC-CNUP1-1
B. robillardoides Tassi, Bollettino del Laboratorio de Orto Botanico Reale Universita Siena 3: 5 (1900) (Table 3, Figure 5).
Table 3.
Characteristics | Present isolate | B. robillardoidesa |
---|---|---|
Conidiogenous cell | Cylindrical to subcylindrical, ampuliform, measured 8.4–11.3×2.5–3.8μm | Ampulliform, hyaline, thin-walled, smooth, measured 4–8×3–4.5μm |
Conidia | Subcylindrical to slightly curved fusoid, 4-septate, measured 18.3–24.2×3.0–3.8μm | Subcylindrical, 4-septate, smooth, slightly constricted at the septa, measured (19–) 21–24(–27)×3–4μm |
Apical appendage | Three-branched, 12.4–18.2μm long | Three-branched, measured (15–)16–20(–22) μm long |
Basal appendage | Single, unbranched, filiform, excentric, 3.8–7.3μm long | Single, unbranched, filiform, flexuous, excentric, 4–7μm long |
aFrom the description by Crous et al. [16].
≡Seimatosporium robillardoides (Tassi) Arx, The genera of fungi sporulating in pure culture: 224 (1981).
Description: Colonies of the strain grew rapidly on PDA, were greyish, and reached 80–83mm in diameter after 14d culture at 25°C. Conidiomata were globose or subglobose, appearing black to brownish black, and measured 276.7–482.2×228.1–364.8μm. Conidiophores were reduced to conidiogenous cells, which were hyaline, cylindrical to subcylindrical, ampuliform, measured 8.4–11.3×2.5–3.8μm, and were formed from the inner cells of the peridial wall. Conidia were subcylindrical to slightly curved fusoid, basal cell obconic with a truncate base, 4-septate, and measured 18.3–24.2×3.0–3.8μm. The apical appendage was 12.4–18.2μm long and three-branched. The basal appendage was 3.8–7.3μm long, single, unbranched, filiform, and excentric.
3.2.3. Taxonomy of CNUFC-NDR3-1
C. carteri X. Wei Wang, Houbraken & Samson, Studies in Mycology 84: 179 (2016) (Table 4, Figure 6).
Table 4.
Characteristics | Present isolate | C. carteria |
---|---|---|
Ascomata | Globose to subglobose, 81–364.5×78–247.9 µm | Globose to subglobose, 175–320×110–220 µm |
Ascomatal hair | 3–5 µm diameter at the base, tapering and fading towards the tips | 4–8.5μm near the base, tapering and fading towards the nearly hyaline tips |
Asci | Fasciculate, clavate or slightly fusiform, contained seven to eight ascospores, measured 16.5–31.5×7.8–10.8 µm | Fasciculate, clavate or slightly fusiform, eight ascospores, measured 17–26×8.5–11.5μm |
Ascospores | Brown, limoniform, usually biapiculate at both ends, measured 5.0–6.7×4.5–5.5 µm | Olivaceous when mature, limoniform, usually biapiculate at both ends, bilaterally flattened, measured (4.5–)5–6(–7.5)×4.4–5μm |
aFrom the description by Wang et al. [23].
Description: Colonies of this strain grew moderately slowly on PDA, reaching 35–37mm in diameter after 7d incubation at 25°C. The colony color was pale yellowish and then became greenish/olivaceous with age. Ascomata were globose to subglobose, and measured 81–364.5×78–247.9µm. Ascomatal hair were 3–5µm diameter at the base, tapering and fading towards the tip. Asci were fasciculate, clavate, or slightly fusiform, contained seven to eight ascospores, and measured 16.5–31.5×7.8–10.8µm. Ascospores were brown, limoniform, usually biapiculate at both ends, and measured 5.0–6.7×4.5–5.5µm.
4. Discussion
The use of DNA sequences has dramatically increased the number of fungal species being recognized and identified [38,39]. Especially the ITS-5.8S rDNA sequences have become important features for the rapid identification of fungi [40,41]. The LSU region on its own or in combination with the ITS region is also valuable in identifying fungi at the intermediate taxonomic level [41,42].
Phylogenetic analysis based on ITS and 28S sequences showed that CNUFC-YR357-1 and CNUFC-YR357-2 strains were clustered within the same clade as A. luteoalbus from NCBI (Figure 1). The results of our molecular data analysis were consistent with the phylogeny presented by Grum-Grzhimaylo et al. [43]. The morphological characteristics of the A. luteoalbus isolate studied were generally similar to those previously described by Zare et al. [10], who transferred this species to genus Acrostalagmus from genus Verticillium, based on their molecular studies. Species of A. luteoalbus have been reported to produce two new indole diketopiperazines, namely luteoalbusins 1 and 2, along with eight previously known ones (3–10). These compounds were evaluated for their cytotoxic activities against SF-268, MCF-7, NCI-H460, and HepG-2 cell lines, and compounds 1–5 showed significant cytotoxicity against all four cancer cell lines [44]. Two new epipolythiodioxopiperazines, named chetracins E and F (1 and 2), along with the previously known chetracin C, exhibited cytotoxicity against the five tested cancer cell lines at the low-micromolar or nanomolar IC50 values isolated from A. luteoalbus [45]. A novel alkali-tolerant rhamnosidase was isolated from the soil fungus A. luteoalbus from Argentina [46].
Our analyses of ITS and 28S sequences showed that the strains CNUFC-CNUP1-1 and CNUFC-CNUP1-2 clustered with B. robillardoides CBS 122705 (type species), with well-supported branches, in full agreement with previous studies by Crous et al. [16] and Wanasinghe et al. [19] (Figure 2). The CNUFC-CNUP1-1 isolate was morphologically most similar to B. robillardoides, as described by Crous et al. [16]. B. robillardoides, B. laurina, and B. rosicola have 4-septate conidia. However, there is significant morphological variation in the conidial measurement; B. robillardoides has a conidia length/width ratio of 6.4 [16]; B. laurina has a conidia length/width ratio of 7.4 [47]; B. rosicola has a conidia length/width ratio of 3.8 [19]. Some Bartalinia species have been recorded as plant pathogens that cause diseases on economically important crops [22]; while some species, such as B. robillardoides, are well known for their secondary metabolites used in pharmaceutical industry. Hence, it is necessary to explore the biodiversity of Bartalinia species in Korea.
Phylogenetic analysis based on ITS and 28S sequences showed that CNUFC-NDR3-1 clustered within the same clade as C. carteri CBS 128.85 (type species) (Figure 3). The morphological features of our isolates corresponded well with the description of C. carteri by Wang et al. [23]. However, our observations showed that the CNUFC-NDR3-1 isolate produces seven to eight ascospores per ascus, whereas the ascus of C. carteri CBS 128.85 produces eight ascospores, as described by Wang et al. [23]. Our results suggest that different isolates of the same species of C. carteri have different number of ascospores. Eight ascospores in each ascus are frequently occurring in comparison to seven ascospores (rare). This species is also showed to produce metabolite such as cochliodinol B and prenisatin [23].
This study significantly improved our understanding of the rare ascomycete genera Acrostalagmus, Bartalinia, and Collariella in freshwater from Korea. There are numerous unknown freshwater derived species still awaiting description. In addition, three species obtained from this study may potentially be highly valuable. Thus, the potential biological activities of A. luteoalbus, B. robillardoides, and C. carteri should be further studied.
Funding Statement
This work was in part supported by the Graduate Program for the Undiscovered Taxa of Korea, and in part by the Project on Survey and Discovery of Indigenous Fungal Species of Korea funded by NIBR and Project on Discovery of Fungi from Freshwater and Collection of Fungarium funded by NNIBR of the Ministry of Environment (MOE), and in part carried out with the support of Cooperative Research Program for Agriculture Science and Technology Development (PJ013744), Rural Development Administration, Republic of Korea. This work was in part supported by the BK21 plus program through the National Research Foundation (NRF) funded by the Ministry of Education of Korea.
Disclosure statement
No potential conflict of interest was reported by the authors.
References
Articles from Mycobiology are provided here courtesy of Korean Society of Mycology
Full text links
Read article at publisher's site: https://doi.org/10.1080/12298093.2018.1550894
Read article for free, from open access legal sources, via Unpaywall: https://www.tandfonline.com/doi/pdf/10.1080/12298093.2018.1550894?needAccess=true&
Citations & impact
Impact metrics
Citations of article over time
Alternative metrics
Discover the attention surrounding your research
https://www.altmetric.com/details/147650046
Smart citations by scite.ai
Explore citation contexts and check if this article has been
supported or disputed.
https://scite.ai/reports/10.1080/12298093.2018.1550894
Article citations
The potential of Hungarian bauxite residue isolates for biotechnological applications.
Biotechnol Rep (Amst), 41:e00825, 20 Dec 2023
Cited by: 0 articles | PMID: 38225962 | PMCID: PMC10788403
In Search of Clinical Markers: Indicators of Exposure in Dampness and Mold Hypersensitivity Syndrome (DMHS).
J Fungi (Basel), 9(3):332, 07 Mar 2023
Cited by: 0 articles | PMID: 36983500 | PMCID: PMC10052403
Two New Species and Three New Records of Ascomycetes in Korea.
Mycobiology, 50(1):30-45, 24 Feb 2022
Cited by: 4 articles | PMID: 35291599 | PMCID: PMC8890549
Fungal diversity notes 1512-1610: taxonomic and phylogenetic contributions on genera and species of fungal taxa.
Fungal Divers, 117(1):1-272, 01 Jan 2022
Cited by: 14 articles | PMID: 36852303 | PMCID: PMC9948003
Six Newly Recorded Fungal Taxa from Freshwater Niche in Korea.
Mycobiology, 49(2):105-121, 29 Dec 2020
Cited by: 0 articles | PMID: 37970186 | PMCID: PMC10635171
Go to all (6) article citations
Data
Data behind the article
This data has been text mined from the article, or deposited into data resources.
BioStudies: supplemental material and supporting data
Nucleotide Sequences (Showing 99 of 99)
- (2 citations) ENA - KP050692
- (2 citations) ENA - KJ710438
- (2 citations) ENA - KX976742
- (2 citations) ENA - KX976747
- (2 citations) ENA - KJ710460
- (2 citations) ENA - KJ443145
- (1 citation) ENA - LM652443
- (1 citation) ENA - MG828872
- (1 citation) ENA - AF382383
- (1 citation) ENA - MG828990
- (1 citation) ENA - KJ443279
- (1 citation) ENA - EU552163
- (1 citation) ENA - MH482853
- (1 citation) ENA - MH482852
- (1 citation) ENA - MH482851
- (1 citation) ENA - KJ443270
- (1 citation) ENA - MH482850
- (1 citation) ENA - MH482856
- (1 citation) ENA - MH482855
- (1 citation) ENA - MH482854
- (1 citation) ENA - KJ443275
- (1 citation) ENA - MG828988
- (1 citation) ENA - KJ443278
- (1 citation) ENA - KJ443277
- (1 citation) ENA - FJ224116
- (1 citation) ENA - KJ443274
- (1 citation) ENA - KJ443273
- (1 citation) ENA - KX976738
- (1 citation) ENA - KX976739
- (1 citation) ENA - KJ443148
- (1 citation) ENA - FJ794472
- (1 citation) ENA - KJ443269
- (1 citation) ENA - KJ443147
- (1 citation) ENA - KJ443268
- (1 citation) ENA - KP757751
- (1 citation) ENA - KJ443149
- (1 citation) ENA - KU556132
- (1 citation) ENA - EU552102
- (1 citation) ENA - MH482846
- (1 citation) ENA - MH482845
- (1 citation) ENA - KU945962
- (1 citation) ENA - KX976741
- (1 citation) ENA - MH482849
- (1 citation) ENA - KX976740
- (1 citation) ENA - MH482848
- (1 citation) ENA - KX976743
- (1 citation) ENA - MH482847
- (1 citation) ENA - KX976745
- (1 citation) ENA - KX976744
- (1 citation) ENA - KX976746
- (1 citation) ENA - KX976749
- (1 citation) ENA - KX976748
- (1 citation) ENA - GU180632
- (1 citation) ENA - AF382369
- (1 citation) ENA - DQ825977
- (1 citation) ENA - AF543786
- (1 citation) ENA - EF543826
- (1 citation) ENA - KX976750
- (1 citation) ENA - DQ278912
- (1 citation) ENA - HG380436
- (1 citation) ENA - DQ278914
- (1 citation) ENA - KJ767127
- (1 citation) ENA - AF452047
- (1 citation) ENA - DQ278927
- (1 citation) ENA - DQ278929
- (1 citation) ENA - KX976642
- (1 citation) ENA - KX976641
- (1 citation) ENA - KX976644
- (1 citation) ENA - KX976646
- (1 citation) ENA - KX976648
- (1 citation) ENA - KX976647
- (1 citation) ENA - KX216521
- (1 citation) ENA - KX976649
- (1 citation) ENA - KJ869149
- (1 citation) ENA - KX216520
- (1 citation) ENA - AF405302
- (1 citation) ENA - AY489737
- (1 citation) ENA - KX976651
- (1 citation) ENA - KX976650
- (1 citation) ENA - KX976653
- (1 citation) ENA - KX216518
- (1 citation) ENA - KX976652
- (1 citation) ENA - KX216519
- (1 citation) ENA - KX976655
- (1 citation) ENA - KX976654
- (1 citation) ENA - JX158443
- (1 citation) ENA - GU180646
- (1 citation) ENA - KM199306
- (1 citation) ENA - JQ044445
- (1 citation) ENA - KJ443144
- (1 citation) ENA - KP757753
- (1 citation) ENA - KU645988
- (1 citation) ENA - KP757754
- (1 citation) ENA - KJ443140
- (1 citation) ENA - KJ869206
- (1 citation) ENA - KJ443139
- (1 citation) ENA - KJ443138
- (1 citation) ENA - JX158421
- (1 citation) ENA - AF104926
Show less
Similar Articles
To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.
Phylogenetic Status of Two Undescribed Zygomycete Species from Korea: Actinomucor elegans and Mucor minutus.
Mycobiology, 45(4):344-352, 31 Dec 2017
Cited by: 4 articles | PMID: 29371802 | PMCID: PMC5780366
Isolation and Characterization of Three Zygomycetous Fungi in Korea: Backusella circina, Circinella muscae, and Mucor ramosissimus.
Mycobiology, 46(4):317-327, 21 Dec 2018
Cited by: 7 articles | PMID: 30637140 | PMCID: PMC6319469
Six Newly Recorded Fungal Taxa from Freshwater Niche in Korea.
Mycobiology, 49(2):105-121, 29 Dec 2020
Cited by: 0 articles | PMID: 37970186 | PMCID: PMC10635171
Characterization of Three Species of Sordariomycetes Isolated from Freshwater and Soil Samples in Korea.
Mycobiology, 47(1):20-30, 14 Feb 2019
Cited by: 5 articles | PMID: 30988988 | PMCID: PMC6450575
Four New Records of Ascomycete Species from Korea.
Mycobiology, 46(4):328-340, 17 Dec 2018
Cited by: 0 articles | PMID: 30637141 | PMCID: PMC6319456
Funding
Funders who supported this work.
Cooperative Research Program for Agriculture Science and Technology Development (1)
Grant ID: PJ0137442018