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Wallemia peruviensis sp. nov., a new xerophilic fungus from an agricultural setting in South America

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Abstract

We obtained four isolates of the xerophilic genus Wallemia from the rooftop of a house made of red brick and cement in an agronomic field planted with common beans and maize in Pachacamac, Lima, Peru. Bayesian phylogenetic analysis with rDNA gene sequences showed these Wallemia isolates form a distinct and strongly supported clade closely related to W. hederae. We examined the macro and micromorphology, growth rate and production of exudates of isolates on media containing different amounts of glucose and NaCl (water activity from 0.9993 to 0.8480). Their chaotropic and kosmotropic tolerance were tested on media with multiple molar concentrations of MgCl2 and MgSO4 (water activity from 0.9880 to 0.7877). Isolates are xerophilic and halotolerant, growing on 17% NaCl-supplemented media (water activity = 0.8480). Maximum concentrations of MgCl2 and MgSO4 at which growth was observed were 1.7 and 3.5 M, respectively. Isolates were shown to represent a novel species, described as Wallemia peruviensis sp. nov. In contrast to W. hederae, W. peruviensis does not produce exudates on malt extract agar + 17% NaCl media. An updated dichotomous key to Wallemia species is provided. This is the first new species of Wallemia described from South America and the first association of a Wallemia species with an agricultural environment on this continent.

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Abbreviations

a w :

Water activity

ITS:

Internal transcribed spacer region rDNA

SSU:

Small subunit 18S rDNA

MCMC:

Markov chain Monte Carlo

MEA:

Malt extract agar

MYA:

Malt yeast extract agar

References

  • Cole GT, Samson RA (1979) Patterns of development in conidial fungi. Pitman, London

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Hoog S, Zalar P, van den Ende BG, Gunde-Cimerman N (2005) Relation of halotolerance to human-pathogenicity in the fungal tree of life: an overview of ecology and evolution under stress. In: Gunde-Cimerman N, Oren A, Plemenitas A (eds) Adaptation to life at high salt-concentration in Archaea, Bacteria and Eukarya. Springer, Dordrecht, pp 373–395

    Google Scholar 

  • de Mendiburu Delgado F (2009) Una herramienta de análisis estadístico para la investigación agrícola. Master’s Thesis, Universidad Nacional de Ingeniería, Lima, Peru

  • Frank M, Kingston E, Jeffery JC, Moss MO, Murray M, Simpson TJ, Sutherland A (1999) Walleminol and walleminone, novel caryophyllenes from the toxigenic fungus Wallemia sebi. Tetrahedron Lett 40:133–136. doi:10.1016/S0040-4039(98)80039-7

    Article  CAS  Google Scholar 

  • Fröhlich-Nowoisky J, Pickersgill DA, Després VR, Pöschl U (2009) High diversity of fungi in air particulate matter. Proc Natl Acad Sci USA 106:12814–12819. doi:10.1073/pnas.0811003106

    Article  PubMed  PubMed Central  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  PubMed  Google Scholar 

  • Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. doi:10.1093/molbev/msp259

    Article  CAS  PubMed  Google Scholar 

  • Guarro J, Gugnani HC, Sood N, Batra R, Mayayo E, Gené J, Kakkar S (2008) Subcutaneous phaeohyphomycosis caused by Wallemia sebi in an immunocompetent host. J Clin Microbiol 46:1129–1131. doi:10.1128/JCM.01920-07

    Article  PubMed  PubMed Central  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi:10.1080/10635150390235520

    Article  PubMed  Google Scholar 

  • Gunde-Cimerman N, Ramos J, Plemenitas A (2009) Halotolerant and halophilic fungi. Mycol Res 113:1231–1241. doi:10.1016/j.mycres.2009.09.002

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hanhela R, Louhelainen K, Pasanen A-L (1995) Prevalence of microfungi in Finnish cow barns and some aspects of the occurrence of Wallemia sebi and Fusaria. Scand J Work Environ Health 21:223–228

    Article  CAS  PubMed  Google Scholar 

  • Jančič S, Nguyen HDT, Frisvad JC, Zalar P, Schroers H-J, Seifert KA, Gunde-Cimerman N (2015) A taxonomic revision of the Wallemia sebi species complex. PLoS One 10:e0125933. doi:10.1371/journal.pone.0125933

    Article  PubMed  PubMed Central  Google Scholar 

  • Jančič S, Frisvad JC, Kocev D, Gostinčar C, Džeroski S, Gunde-Cimerman N (2016a) Production of secondary metabolites in extreme environments: food- and airborne Wallemia spp. produce toxic metabolites at hypersaline conditions. PLoS One 11:e0169116. doi:10.1371/journal.pone.0169116

    Article  PubMed  PubMed Central  Google Scholar 

  • Jančič S, Zalar P, Kocev D, Schroers H-J, Džeroski S, Gunde-Cimerman N (2016b) Halophily reloaded: new insights into the extremophilic life-style of Wallemia with the description of Wallemia hederae sp. nov. Fungal Divers 76:97–118. doi:10.1007/s13225-015-0333-x

    Article  Google Scholar 

  • Johan-Olsen O (1887) Om sop på klipfisk den såkaldte mid. Christ Vidensk Forh 12:1–20

    Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi:10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matheny PB, Gossmann JA, Zalar P, Kumar TKA, Hibbett DS (2006) Resolving the phylogenetic position of the Wallemiomycetes: an enigmatic major lineage of Basidiomycota. Can J Bot 84:1794–1805. doi:10.1139/b06-128

    Article  CAS  Google Scholar 

  • Munsell Color Company (1954) Munsell soil color charts, 1954th edn. Munsell Color Company, Baltimore

    Google Scholar 

  • Nguyen HDT, Jančič S, Meijer M, Tanney JB, Zalar P, Gunde-Cimerman N, Seifert KA (2015) Application of the phylogenetic species concept to Wallemia sebi from house dust and indoor air revealed by multi-locus genealogical concordance. PLoS One 10:e0120894. doi:10.1371/journal.pone.0120894

    Article  PubMed  PubMed Central  Google Scholar 

  • Padamsee M, Kumar TKA, Riley R, Binder M, Boyd A, Calvo AM, Furukawa K, Hesse C, Hohmann S, James TY, LaButti K, Lapidus A, Lindquist E, Lucas S, Miller K, Shantappa S, Grigoriev IV, Hibbett DS, McLaughlin DJ, Spatafora JW, Aime MC (2012) The genome of the xerotolerant mold Wallemia sebi reveals adaptations to osmotic stress and suggests cryptic sexual reproduction. Fungal Genet Biol 49:217–226. doi:10.1016/j.fgb.2012.01.007

    Article  CAS  PubMed  Google Scholar 

  • Pitt JI (1975) Xerophilic fungi and the spoilage of foods of plant origin. In: Duckworth RB (ed) Water relations of food. Academic Press, London, pp 273–307

    Chapter  Google Scholar 

  • Pitt JI, Hocking AD (2009) Fungi and food spoilage, 3rd edn. Springer, Sydney

    Book  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O (2000) Introduction to food- and airborne fungi, 6th edn. Centraalbureau voor Schimmelcultures, Wageningen

    Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. doi:10.1038/nmeth.2089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi T (1997) Airborne fungal colony-forming units in outdoor and indoor environments in Yokohama, Japan. Mycopathologia 139:23–33. doi:10.1023/A:1006831111595

    Article  CAS  PubMed  Google Scholar 

  • Takatori K, Lee H-J, Ohta T, Shida T (1994) Composition of the house dust mycoflora in Japanese houses. In: Samson RA, Flannigan B, Flannigan ME, Verhoeff AP, Adan OCG, Hoekstra ES (eds) Health implications of fungi in indoor environments. Elsevier, Berlin, pp 93–101

    Google Scholar 

  • von Arx JA (1970) The genera of fungi sporulating in pure culture, 1st edn. Gantner Verlag KG, Leutershausen

    Google Scholar 

  • Walther G, Garnica S, Weiß M (2005) The systematic relevance of conidiogenesis modes in the gilled Agaricales. Mycol Res 109:525–544. doi:10.1017/S0953756205002868

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Wilson K, Padhye AA, Carmichael JW (1969) Antifungal activity of Wallemia ichthyophaga (=Hemispora stellata Vuill.=Torula epizoa Corda). Antonie Van Leeuwenhoek 35:529–532. doi:10.1007/BF02219170

    Article  CAS  PubMed  Google Scholar 

  • Wood GM, Mann PJ, Lewis DF, Reid WJ, Moss MO (1990) Studies on a toxic metabolite from the mould Wallemia. Food Addit Contam 7:69–77. doi:10.1080/02652039009373822

    Article  CAS  PubMed  Google Scholar 

  • Zajc J, Zalar P, Sepcic K, Gunde-Cimerman N (2011) Xerophilic fungal genus Wallemia: bioactive inhabitants of marine solar salterns and salty food. Zb Matice Srp za Prir Nauk 120:7–18. doi:10.2298/ZMSPN1120007Z

    Article  Google Scholar 

  • Zajc J, Liu Y, Dai W, Yang Z, Hu J, Gostinčar C, Gunde-Cimerman N (2013) Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genom 14:617–630. doi:10.1186/1471-2164-14-617

    Article  CAS  Google Scholar 

  • Zajc J, Džeroski S, Kocev D, Oren A, Sonjak S, Tkavc R, Gunde-Cimerman N (2014a) Chaophilic or chaotolerant fungi: a new category of extremophiles? Front Microbiol 5:1–15. doi:10.3389/fmicb.2014.00708

    Article  Google Scholar 

  • Zajc J, Kogej T, Galinski EA, Ramos J, Gunde-Cimermana N (2014b) Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl Environ Microbiol 80:247–256. doi:10.1128/AEM.02702-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalar P, de Hoog GS, Schroers H-J, Frank JM, Gunde-Cimerman N (2005) Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie Van Leeuwenhoek 87:311–328. doi:10.1007/s10482-004-6783-x

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank David Aime for facilitating sampling in Peru and Daniel Reátegui for collecting isolates. We also thank Beth Kennedy for testing selective media, John Klimek for culture maintenance, Marlon Rodríguez for preparing some of the media used in this study, and rest of the members of the Aime lab for constructive comments on the manuscript. Special thanks to Dr. Jozef Kokini at the Department of Food Science, Purdue University, for facilitating the use of the aw-meter, and to Luis Maldonado and José Bonilla for technical help. Finally, we thank SERFOR, Peru for granting permits to collect and work with fungal taxa from the country and two anonymous reviewers for suggesting improvements to this manuscript.

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Correspondence to M. Catherine Aime.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1 Media used in this study (PDF 215 kb)

Online Resource 2 Bayesian phylogenetic trees of ITS and SSU datasets of Wallemia isolates (PDF 139 kb)

Online Resource 3 Colony characteristics of Wallemia peruviensis at 15 days of growth (PDF 221 kb)

792_2017_960_MOESM4_ESM.docx

Online Resource 4 Growth of Wallemia peruviensis under kosmotropic (MgSO4) and chaotropic (MgCl2) solutes at different molar concentrations (DOCX 2456 kb)

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Díaz-Valderrama, J.R., Nguyen, H.D.T. & Aime, M.C. Wallemia peruviensis sp. nov., a new xerophilic fungus from an agricultural setting in South America. Extremophiles 21, 1017–1025 (2017). https://doi.org/10.1007/s00792-017-0960-0

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