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Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica

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Abstract

We surveyed the diversity, distribution and ecology of non-lichenised fungal communities associated with the Antarctic lichens Usnea antarctica and Usnea aurantiaco-atra across Antarctica. The phylogenetic study of the 438 fungi isolates identified 74 taxa from 21 genera of Ascomycota, Basidiomycota and Zygomycota. The most abundant taxa were Pseudogymnoascus sp., Thelebolus sp., Antarctomyces psychrotrophicus and Cryptococcus victoriae, which are considered endemic and/or highly adapted to Antarctica. Thirty-five fungi may represent new and/or endemic species. The fungal communities displayed high diversity, richness and dominance indices; however, the similarity among the communities was variable. After discovering rich and diverse fungal communities composed of symbionts, decomposers, parasites and endemic and cold-adapted cosmopolitan taxa, we introduced the term “lichensphere”. We hypothesised that the lichensphere may represent a protected natural microhabitat with favourable conditions able to help non-lichenised fungi and other Antarctic life forms survive and disperse in the extreme environments of Antarctica.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arenz BE, Blanchette RA (2011) Distribution and abundance of soil fungi in Antarctica at sites on the Peninsula, Ross Sea Region and McMurdo Dry Valleys. Soil Biol Biochem 43:308–315

    Article  CAS  Google Scholar 

  • Arenz BE, Held BW, Jurgens JA, Farrell RL, Blanchette RA (2006) Fungal diversity in soils and historic wood from the Ross Sea Region of Antarctica. Soil Biol Biochem 38:3057–3064

    Article  CAS  Google Scholar 

  • Bacon CW, White JF (2000) Biology and evolution of microbial endophytes. Dekker, New York

    Google Scholar 

  • Bridge PD, Spooner BM (2012) Non-lichenized Antarctic fungi: transient visitors or members of a cryptic ecosystem? Fungal Ecol 5:381–394

    Article  Google Scholar 

  • Brunati M, Rojas JL, Sponga F, Ciciliato I, Losi D, Göttlich E et al (2009) Diversity and pharmaceutical screening of fungi from benthic mats of Antarctic lakes. Mar Genomics 2:43–50

    Article  PubMed  Google Scholar 

  • de Hoog GS, Göttlich E, Platas G, Genilloud O, Leotta G, Van Brummelen J (2005) Evolution, taxonomy and ecology of the genus Thelebolus in Antarctica. Stud Mycol 51:33–76

    Google Scholar 

  • Furbino LE, Godinho VM, Santiago IF, Pellizari FM, Alves TMA, Zani CL et al (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microb Ecol 67:775–787

    Article  PubMed  Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330

    PubMed Central  CAS  PubMed  Google Scholar 

  • Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya N, Pupo D et al (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Godinho VM, Gonçalves VN, Santiago IF, Figueredo HM, Vitoreli GA, Schaefer CEGR et al (2014) Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles. doi:10.1007/s00792-015-0741-6 (in press)

    Google Scholar 

  • Gonçalves VN, Vaz ABM, Rosa CA, Rosa LH (2012) Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol Ecol 82:459–471

    Article  PubMed  Google Scholar 

  • Gonçalves VN, Campos LS, Melo IS, Pellizari VH, Rosa CA, Rosa LH (2013) Penicillium solitum: a mesophilic, psychrotolerant fungus present in marine sediments from Antarctica. Polar Biol 36:1823–1831

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Paleontol Electron 4:1–9

    Google Scholar 

  • Harutyunyan S, Muggia L, Grube M (2008) Black fungi in lichens from seasonally arid habitats. Stud Mycol 61:83–90

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Houbraken J, Frisvad JC, Seifert KA, Overy DP, Tuthill DM, Valdez JG et al (2012) New penicillin-producing Penicillium species and an overview of section Chrysogena. Persoonia 29:78–100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CAB International, Wallingford

    Google Scholar 

  • Kobayasi Y, Hiratsuka N, Korf RP, Tubaki K, Aoshima K, Soneda M et al (1967) Mycological studies of the Alaskan Arctic. Res Commun Inst Ferment Osaka 3:1–138

    Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam

    Google Scholar 

  • Lachance MA, Bowles JM, Starmer WT, Barker JS (1999) Kodamaea kakaduensis and Candida tolerans, two new ascomycetous yeast species from Australian hibiscus flowers. Can J Microbiol 45:172–177

    Article  CAS  PubMed  Google Scholar 

  • Li WC, Zhou J, Guo SY, Guo LD (2007) Endophytic fungi associated with lichens in Baihua mountain of Beijing, China. Fungal Divers 25:69–80

    Google Scholar 

  • Loque CP, Medeiros AO, Pellizzari FM, Oliveira EC, Rosa CA, Rosa LH (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648

    Article  Google Scholar 

  • Lorch JM, Lindner DL, Gargas A, Muller LK, Minnis AM, Blehert DS (2013) A culture-based survey of fungi in soil from bat hibernacula in the eastern United States and its implications for detection of Geomyces destructans, the causal agent of bat white-nose syndrome. Mycologia 105:237–252

    Article  CAS  PubMed  Google Scholar 

  • Mercantini R, Marsella R, Cervellati MC (1989) Keratinophilic fungi isolated from Antarctic soil. Mycopathologia 106:47–52

    Article  CAS  PubMed  Google Scholar 

  • Minnis AM, Lindner DL (2013) Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 117:638–649

    Article  PubMed  Google Scholar 

  • Möller C, Dreyfuss MM (1996) Microfungi from Antarctic lichens, mosses and vascular plants. Mycology 88:922–933

    Article  Google Scholar 

  • Montemartini A, Caretta G, Del Frate G (1993) Notes on Thelebolus microsporus isolated in Antarctica. Mycotaxon 48:343–358

    Google Scholar 

  • Nelson PE, Dignani MC, Anaissie EJ (1994) Taxonomy, biology, and clinical aspects of Fusarium species. Clin Microbiol Rev 7:479–504

    PubMed Central  CAS  PubMed  Google Scholar 

  • Petrini O, Hake U, Dreyfuss MM (1990) An analysis of fungal communities isolated from fruticose lichens. Mycologia 82:444–451

    Article  Google Scholar 

  • Renker C, Zobel M, Öpik M, Allen MF, Allen EB, Vosátka M et al (2004) Structure, dynamics, and restoration of plant communities: do arbuscular mycorrhizae matter? In: Temperton VM, Hobbs RJ, Nuttle T, Halle S (eds) Assembly rules and restoration ecology—bridging the gap between theory and practice. Island Press, Washington, DC, pp 189–229

    Google Scholar 

  • Rosa LH, Vaz ABM, Caligiorne RB, Campolina S, Rosa CA (2009) Endophytic fungi associated with the Antarctic Grass Deschampsia antarctica Desv. (Poaceae). Polar Biol 32:161–167

    Article  Google Scholar 

  • Rosa LH, Vieira MLA, Santiago IF, Rosa CA (2010) Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol 73:178–189

    CAS  PubMed  Google Scholar 

  • Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141

    Article  Google Scholar 

  • Spielmann AA, Pereira AB (2012) Lichens of the maritime Antarctica. Glalia 4:1–28

    Google Scholar 

  • Stchigel AM, Cano J, MacCormack CW (2001) Antarctomyces psychrotrophicus gen. et sp. nov., a new ascomycete from Antarctica. Mycol Res 105:377–382

    Article  CAS  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 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tosi S, Del Frate G, Gerdol R, Caretta G (2002) Fungi isolated from Antarctic mosses. Polar Biol 25:262–268

    Google Scholar 

  • Upson R, Newsham KK, Bridge PD, Pearce DA, Read DJ (2009) Taxonomic affinities of dark septate root endophytes of Colobanthus quitensis and Deschampsia antarctica, the two native Antarctic vascular plant species. Fungal Ecol 2:184–196

    Article  Google Scholar 

  • Vaz ABM, Rosa LH, Vieira MLA, Garcia V, Brandão LR, Teixeira LCRS et al (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 42:937–947

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vishniac HS (2006) Yeast biodiversity in the Antarctic. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer-Verlag, Berlin, pp 221–240

    Google Scholar 

  • White TJ, Bruns TD, Lee SB (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis NA, Gelfand J, Sninsky J et al (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Yarrow D (1998) Methods for the isolation, maintenance and identification of yeast. In: Kurtzman CP, Fell JW (eds) The yeasts: a taxonomic study. Elsevier, Amsterdam

    Google Scholar 

  • Zhang T, Zhang YQ, Liu HY, Wei YZ, Li HL, Su J et al (2013) Diversity and cold adaptation of culturable endophytic fungi from bryophytes in the Fildes Region, King George Island, maritime Antarctica. FEMS Microbiol Lett 341:52–61

    Article  CAS  PubMed  Google Scholar 

  • Zucconi L, Selbmann L, Buzzini P, Turchetti B, Guglielmin M, Frisvad JC et al (2012) Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol 35:749–757

    Article  Google Scholar 

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Acknowledgments

We acknowledge the financial support from CNPq PROANTAR 407230/2013-0 and INCT Criosfera. We also thank Dr. A. F. Spielmann for the lichen identifications.

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Authors and Affiliations

  1. Laboratory of Systematic and Biomolecules of Fungi, Departamento de Microbiologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, CEP 31270-901, Brazil

    Iara F. Santiago, Marco Aurélio Soares, Carlos A. Rosa & Luiz H. Rosa

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  1. Iara F. Santiago
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  2. Marco Aurélio Soares
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  3. Carlos A. Rosa
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  4. Luiz H. Rosa
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Correspondence to Luiz H. Rosa.

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We declare no conflict of interest among the authors.

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Communicated by M. da Costa.

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Santiago, I.F., Soares, M.A., Rosa, C.A. et al. Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19, 1087–1097 (2015). https://doi.org/10.1007/s00792-015-0781-y

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