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Aspergillus atacamensis and A. salisburgensis: two new halophilic species from hypersaline/arid habitats with a phialosimplex-like morphology

Extremophiles volume 21, pages 755–773 (2017)Cite this article

Abstract

Halophilic fungal strains isolated from historical wooden staircase in a salt mine in Austria, and from wall biofilm and soil of a cave in the Coastal Range of the hyperarid Atacama Desert in Chile were characterised and described newly as Aspergillus salisburgensis and Aspergillus atacamensis. Morphological characters including solitary phialides producing solitary conidia and conidia in chains and/or heads suggested affinity to Aspergillus subgenus Polypaecilum. Strains required salt for growth, grew optimally on media with 10–25% NaCl and at 15–28 °C. These values are similar to those observed for Aspergillus salinarus comb. nov. (Phialosimplex salinarum), while the ex-type strains of Aspergillus sclerotialis, Aspergillus chlamydosporus and Aspergillus caninus (all belonging to Aspergillus subgen. Polypaecilum) grew optimally at 0–5% NaCl and showed fastest growth at 28–37 °C. Phylogenetic analyses on the basis of rDNA sequences, RAPD-PCR fingerprint patterns, and cellobiohydrolase gene (cbh-I) polymorphism clustered the strains into three groups and supported their taxonomic recognition as A. salinarus, A. atacamensis and A. salisburgensis. On the basis of phylogenetic inferences, also Sagenomella keratitidis is newly combined as Aspergillus keratitidis and inferred as a species of Aspergillus subgenus Polypaecilum.

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References

  • Akopyanz N, Bukanov NO, Westblom TU, Kresovich S, Berg DE (1992) DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucl Acids Res 20:5137–5142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali I, Akbar A, Anwar M, Yanwisetpakdee B, Prasongsuk S, Lotrakul P, Punnapayak H (2014) Purification and characterization of extracellular, polyextremophilic α-amylase obtained from halophilic Engyodontium album. Iran J Biotech 12:e1155. doi:10.15171/ijb.1155

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman JD (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azua-Bustos AC, González-Silva C, Salas L, Palma RE, Vicuña R (2010) A novel subaerial Dunaliella species growing on cave spiderwebs in the Atacama Desert. Extremophiles 14:443–452

    Article  CAS  PubMed  Google Scholar 

  • Brizzio S, Turchetti B, de García V, Libkind D, Buzzini P, van Broock M (2007) Extracellular enzymatic activities of basidiomycetous yeasts isolated from glacial and subglacial waters of northwest Patagonia (Argentina). Can J Microbiol 53:519–525. doi:10.1139/W07-010

    Article  CAS  PubMed  Google Scholar 

  • Buchalo AS, Nevo E, Wasser SP, Oren A, Molitoris HP (1998) Fungal life in the extremely hypersaline water of the Dead Sea: first records. Proc Roy Soc Lond 265:1461–1465

    Article  CAS  Google Scholar 

  • Cole GT, Samson RA (1979) Patterns of development in conidial fungi. Pitman Publishing Ltd. London, San Franzisco, Melbourne

  • Connell L, Staudigel H (2013) Fungal diversity in a dark oligotrophic volcanic ecosystem (DOVE) on Mount Erebus, Antarctica. Biology 2:798–809. doi:10.3390/biology2020798

    Article  PubMed  PubMed Central  Google Scholar 

  • de Hoog GS, Zalar P, van den Ende BG, Gunde-Cimerman N (2005) Relation of halotolerance to human-pathogenicity in the fungal tree of live: an overview of ecology and evolution under stress. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptations to life at high salt concentrations in archaea, bacteria and eukarya. Springer Verlag, New York, pp 185–200

    Google Scholar 

  • Ettenauer J, Sterflinger K, Piñar G (2010) Cultivation and molecular monitoring of halophilic microorganisms inhabiting an extreme environment presented by a salt-attacked monument. Int J Astrobiol 9:59–72

    Article  CAS  Google Scholar 

  • Gams W (1978) Connected and disconnected chains of phialoconidia and Sagenomella gen. nov. segregated from Acremonium. Persoonia 10:97–112

    Google Scholar 

  • Gams W, Verkley GJM, Crous PW (2007) CBS course of mycology. In: 5th edn. CBS-KNAW Fungal Biodiversity Centre, Utrecht

  • Gené J, Blanco JL, Cano J, Garcia ME, Guarro J (2003) New filamentous fungus Sagenomella chlamydospora responsible for a disseminated infection in a dog. J Clin Microbiol 41:1722–1725

    Article  PubMed  PubMed Central  Google Scholar 

  • Gostinčar C, Grube M, de Hoog GS, Zalar P, Gunde-Cimerman N (2010) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71:2–11. doi:10.1111/j.1574-6941.2009.00794.x

    Article  PubMed  Google Scholar 

  • Greiner K, Peršoh D, Weig A, Rambold G (2014) Phialosimplex salinarum, a new species of Eurotiomycetes from a hypersaline habitat. IMA Fungus 5:161–172

    Article  PubMed  PubMed Central  Google Scholar 

  • Gunde-Cimerman N, Zalar P (2014) Extremely halotolerant and halophilic fungi inhabit brine in solar salterns around the globe. Food Technol Biotechnol 52:170–179

    Google Scholar 

  • Gunde-Cimerman N, Zalar P, Hoog SD, Plemenitaš A (2000) Hypersaline water in salterns and natural ecological niches for halophilic black yeast. FEMS Microbiol Ecol 32:235–240

    CAS  Google Scholar 

  • Gunde-Cimerman N, Butinar L, Sonjak S, Turk M, Uršič V, Zalar P, Plemenitaš A (2006) Halotolerant and halophilic fungi from costal environments in the Arctics. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptations to life at high salt concentrations in archaea, bacteria and eukarya. Springer Verlag, New York, pp 397–424

    Google Scholar 

  • Hong SB, Go SJ, Shin H-D, Frisvad J, Samson RA (2005) Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97:1316–1329

    Article  CAS  PubMed  Google Scholar 

  • Houbraken J, Samson RA (2011) Phylogeny of Penicillium and the segregation Trichocomaceae into three families. Stud Mycol 70:1–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houbraken J, de Vries RP, Samson RA (2014) Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. Adv Appl Microbiol 86:199–249. doi:10.1016/B978-0-12-800262-9.00004-4

    Article  PubMed  Google Scholar 

  • Hsieh HM, Ju YM, Hsueh PR, Lin HY, Hu FR, Chen WL (2009) Fungal keratitis caused by a new filamentous hyphomycete Sagenomella keratitidis. Bot Stud 50(3):331–336

    Google Scholar 

  • Jančič S, Zalar P, Kocev D, Schroers H-J, Džeroski S, Gunde-Cimerman N (2015) Halophily reloaded: new insights into the extremophilic life-style of Wallemia with the description of Wallemia hederae sp. nov. Fung Diver. doi:10.1007/s13225-015-0333-x

  • Kang H-W, Park D-S, Go S-J, Eun M-Y (2002) Fingerprinting of diverse genomes using PCR with universal rice primers generated from repetitive sequence of Korean weedy rice. Mol Cells 13:281–287

    CAS  PubMed  Google Scholar 

  • Kauff F, Lutzoni F (2002) Phylogeny of Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Mol Phylogen Evol 25:138–156

    Article  CAS  Google Scholar 

  • Kis-Papo T, Grishkan I, Oren A, Wasser SP, Nevo E (2001) Spatiotemporal diversity of filamentous fungi in the hypersaline Dead Sea. Mycol Res 105:749–756

    Article  Google Scholar 

  • Kocsubé S, Perrone G, Magistà D, Houbraken J, Varga J, Szigeti G, Hubka V, Hong S-B, Frisvad JC, Samson RA (2016) Aspergillus is monophyletic: evidence from multiple gene phylogenies and extrolites profiles. Stud Mycol 85:199–213

    Article  PubMed  PubMed Central  Google Scholar 

  • Kraková L, Chovanová K, Puškarová A, Bučková M, Pangallo D (2012) A novel PCR-based approach for the detection and classification of potential cellulolytic fungal strains isolated from museum items and surrounding indoor environment. Lett Appl Microbiol 54:433–440

    Article  PubMed  Google Scholar 

  • Lenassi M, Gostinčar C, Jackman S, Turk M, Sadowski I, Nislow C, Gunde-Cimerman N, Plemenitaš A (2013) Whole genome duplication and enrichment of metal cation transporters revealed by De Novo genome sequencing of extremely halotolerant black yeast Hortaea werneckii. PLoS One 8(8):e71328. doi:10.1371/journal.pone.0071328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McNeill J, Barrie FR, Buck WR et al (2012) International Code of Nomenclature for algae, fungi, and plants (Melbourne Code). Regnum Vegetabile 154:208

    Google Scholar 

  • Michaelsen A, Pinzari F, Ripka K, Lubitz W, Piñar G (2006) Application of molecular techniques for the identification of fungal communities colonising paper material. Int Biodeterior Biodegrad 58:133–141

    Article  CAS  Google Scholar 

  • O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, Conn, pp 225–233

  • Oren A (2010) Industrial and environmental applications of halophilic microorganisms. Environ Technol 31:825–834. doi:10.1080/09593330903370026

    Article  CAS  PubMed  Google Scholar 

  • Pangallo D, Bučková M, Kraková L, Puškárová A, Šaková N, Grivalský T, Chovanová K, Zemánková M (2014) Biodeterioration of epoxy resin: a microbial survey through culture-independent and culture-dependent approaches. Environ Microbiol 17:462–479. doi:10.1111/1462-2920.12523

    Article  PubMed  Google Scholar 

  • Paterson RRM, Bridge PD (1994) Biochemical techniques for filamentous fungi. IMI Technical Habdbooks, CAB International, Wallingford

  • Piñar G, Piombino-Mascali D, Maixner F, Zink A, Sterflinger K (2013) Microbial survey of the mummies from the Capuchin Catacombs of Palermo, Italy: biodeterioration risk and contamination of the indoor air. FEMS Microbiol Ecol 86:341–356. doi:10.1111/1574-6941.12165

    Article  PubMed  PubMed Central  Google Scholar 

  • Piñar G, Kraková L, Pangallo D, Piombino-Mascali D, Maixner F, Zink A, Sterflinger K (2014) Halophilic bacteria are colonizing the exhibition areas of the Capuchin Catacombs in Palermo, Italy. Extremophiles 18:677–691. doi:10.1007/s00792-014-0649-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Piñar G, Sterflinger K, Pinzari F (2015a) Unmasking the measles-like parchment discoloration: molecular and micro-analytical approach. Environ Microbiol 17:427–443. doi:10.1111/1462-2920.12471

    Article  PubMed  Google Scholar 

  • Piñar G, Tafer H, Sterflinger K, Pinzari F (2015b) Amid the possible causes of a very famous foxing: molecular and microscopic insight into Leonardo da Vinci’s self-portrait. Environ Microbiol Rep 7(6):849–859. doi:10.1111/1758-2229.12313

    Article  PubMed  PubMed Central  Google Scholar 

  • Piñar G, Dalnodar D, Voitl C, Reschreiter H, Sterflinger K (2016) Biodeterioration risk threatens the 3100 year old staircase of hallstatt (Austria): possible involvement of halophilic microorganisms. PLoS One 11(2):e0148279. doi:10.1371/journal.pone.0148279

    Article  PubMed  PubMed Central  Google Scholar 

  • Pitt JI, Hocking AD (1985) Fungi and food spoilage. Academic Press, Sydney

    Google Scholar 

  • Pitt JI, Taylor JW (2014) Aspergillus, its sexual states, and the new International Code of Nomenclature. Mycologia 106:1051–1062. doi:10.3852/14-060

    Article  PubMed  Google Scholar 

  • Pitt JI, Taylor JW (2016) (2441) Proposal to conserve the name Aspergillus (Fungi: Eurotiales: Tr ichocomaceae) with a conserved type to maintain also the name Eurotium. Taxon 65:631–632. doi:10.12705/653.17

    Article  Google Scholar 

  • Ravindran C, Varatharajan GR, Rajasabapathy R, Vijayakanth S, Kumar AH, Meena RM (2012) A role for antioxidants in acclimation of marine derived pathogenic fungus (NIOCC 1) to salt stress. Microb Pathog 53:168–179. doi:10.1016/j.micpath.2012.07.004

    Article  CAS  PubMed  Google Scholar 

  • Ripka K, Denner E, Michaelsen A, Lubitz W, Piñar G (2006) Molecular characterisation of Halobacillus strains isolated from different medieval wall paintings and building materials in Austria. Int Biodeterior Biodegrad 58:124–132. doi:10.1016/j.ibiod.2006.05.004

    Article  CAS  Google Scholar 

  • Rittenour WR, Ciaccio CE, Barnes CS, Kashon ML, Lemons AR, Beezhold DH, Green BJ (2013) Internal transcribed spacer rRNA gene sequencing analysis of fungal diversity in Kansas City indoor environments. Environ Sci Process Impacts 16(1):33–43. doi:10.1039/c3em00441d

    Article  Google Scholar 

  • Romão-Dumaresq AS, Dourado MN, Fávaro LCdL, Mendes R, Ferreira A, Rodrigo Mendes R, Ferreira A, Araújo WL (2016) Diversity of cultivated fungi associated with conventional and transgenic sugarcane and the interaction between endophytic trichoderma virens and the host plant. PLoS One 11(7):e0158974. doi:10.1371/journal.pone.0158974

    Article  PubMed  PubMed Central  Google Scholar 

  • Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CHW, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsube S, Szigeti G, Yaguchi T, Frisvad JC (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173. doi:10.1016/j.simyco.2014.07.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satow MM, Attili-Angelis D, de Hoog GS, Angelis DF, Vicente VA (2008) Selective factors involved in oil flotation isolation of black yeasts from the environment. Stud Mycol 61:157–163. doi:10.3114/sim.2008.61.16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sert HB, Sterflinger K (2010) A new Coniosporium species from historical marble monuments. Mycol Prog 9:353–359. doi:10.1007/s11557-009-0643-z

    Article  Google Scholar 

  • Sigler L, Sutton DA, Gibas CF, Summerbell RC, Noel RK, Iwen PC (2010) Phialosimplex, a new anamorphic genus associated with infections in dogs and having phylogenetic affinity to the Trichocomaceae. Med Mycol 48:35–45. doi:10.3109/13693780903225805

    Article  Google Scholar 

  • Strauss ML, Jolly NP, Lambrechts MG, van Rensburg P (2001) Screening for the production of extracellular hydrolytic enzymes by non Saccharomyces wine yeasts. J Appl Microbiol 91:182–190. doi:10.1046/j.1365-2672.2001.01379.x

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum Parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor JW, Göker M, Pitt JI (2016) Choosing one name for pleomorphic fungi: the example of Aspergillus versus Eurotium, Neosartorya and Emericella. Taxon 65:593–601

    Article  Google Scholar 

  • Tian JJ, GaoX-X Zhang W-M, Wang L, Qu L-H (2013) Molecular identification of endophytic fungi from Aquilaria sinensis and artificial agarwood induced by pinholes-infusion technique. Afr J Biotech 12(21):3115–3131

    CAS  Google Scholar 

  • Welsh J, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18:7213–7218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Williams JG, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535

    Article  CAS  PubMed  PubMed Central  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? Frontiers in microbiology 5:708-1–708-5. doi:10.3389/fmicb.2014.00708

    Article  Google Scholar 

  • Zajc J, Kogej T, Galinski EA, Ramos J, Gunde-Cimerman N (2014b) Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl Environ Microbiol 80(1):247–256. doi:10.1128/AEM.02702-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalar P, de Hoog GS, Gunde-Cimerman N (1999) Ecology of halotolerant dothideaceous black yeasts. Stud Mycol 43:38–48

    Google Scholar 

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

    Article  CAS  Google Scholar 

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Acknowledgements

Dr. K. Greiner is acknowledged for the kind supply of the type strain P. salinarum DSM 27530. Dr. R. Kostanjšek (Infrastructural Centre for Microscopy of Biological Samples, MRIC UL, Slovenia) is acknowledged for the scanning electron micrographs presented in Fig. 7. Armando Azua-Bustos thanks the European Research Council, Starting Grant No. 307496.

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Author notes

  1. Livia Martinelli

    Present address: Reformation and Renaissance Studies (CRRS), Victoria University in the University of Toronto, 71 Queens Park Crescent E, Toronto, Canada

  2. Livia Martinelli and Polona Zalar contributed equally to the work.

Authors and Affiliations

  1. Department of Biotechnology, Vienna Institute of Biotechnology (VIBT), University of Natural Resources and Life Sciences, Muthgasse 11, 1190, Vienna, Austria

    Livia Martinelli, Katja Sterflinger & Guadalupe Piñar

  2. Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, 1000, Ljubljana, Slovenia

    Polona Zalar & Nina Gunde-Cimerman

  3. Instituto de Ciencias Biomédicas, Facultad de Ciencias de la Salud, Universidad Autónoma de Chile, 8910060, Santiago, Chile

    Armando Azua-Bustos

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  1. Livia Martinelli
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  2. Polona Zalar
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Correspondence to Polona Zalar.

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Communicated by A. Oren.

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Martinelli, L., Zalar, P., Gunde-Cimerman, N. et al. Aspergillus atacamensis and A. salisburgensis: two new halophilic species from hypersaline/arid habitats with a phialosimplex-like morphology. Extremophiles 21, 755–773 (2017). https://doi.org/10.1007/s00792-017-0941-3

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Keywords

  • Hypersaline environments
  • Halophilic fungi
  • Phialosimplex-like
  • Aspergillus