Advertisement

Extremophiles

, Volume 22, Issue 3, pp 381–393 | Cite as

Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites

  • Eldon C. Q. Gomes
  • Valéria M. Godinho
  • Débora A. S. Silva
  • Maria T. R. de Paula
  • Gislaine A. Vitoreli
  • Carlos L. Zani
  • Tânia M. A. Alves
  • Policarpo A. S. Junior
  • Silvane M. F. Murta
  • Emerson C. Barbosa
  • Jaquelline G. Oliveira
  • Fabio S. Oliveira
  • Camila R. Carvalho
  • Mariana C. Ferreira
  • Carlos A. Rosa
  • Luiz H. Rosa
Original Paper

Abstract

Molecular biology techniques were used to identify 218 fungi from soil samples collected from four islands of Antarctica. These consisted of 22 taxa of 15 different genera belonging to the Zygomycota, Ascomycota, and Basidiomycota. Mortierella, Antarctomyces, Pseudogymnoascus, and Penicillium were the most frequently isolated genera and Penicillium tardochrysogenum, Penicillium verrucosus, Goffeauzyma gilvescens, and Mortierella sp. 2 the most abundant taxa. All fungal isolates were cultivated using solid-state fermentation to obtain their crude extracts. Pseudogymnoascus destructans, Mortierella parvispora, and Penicillium chrysogenum displayed antiparasitic activities, whilst extracts of P. destructans, Mortierella amoeboidea, Mortierella sp. 3, and P. tardochrysogenum showed herbicidal activities. Reported as pathogenic for bats, different isolates of P. destructans exhibited trypanocidal activities and herbicidal activity, and may be a source of bioactive molecules to be considered for chemotherapy against neglected tropical diseases. The abundant presence of P. destructans in soils of the four islands gives evidence supporting that soils in the Antarctic Peninsula constitute a natural source of strains of this genus, including some P. destructans strains that are phylogenetically close to those that infect bats in North America and Europe/Palearctic Asia.

Keywords

Antarctica Fungi Neglected tropical diseases Mortierella Pseudogymnoascus 

Notes

Acknowledgements

The authors thank the Program for Technological Development of Tools for Health-PDTIS-FIOCRUZ for use of its facilities.

Compliance with ethical standards

Conflict of interest

The authors reported no conflict of interest.

Funding

We acknowledge the financial support from CNPq PROANTAR 407230/o-0, INCT Criosfera, FAPEMIG (0050-13), CAPES (23038.003478/2013-92), PROPP-UFOP and PRPq-UFMG.

Supplementary material

792_2018_1003_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 12 kb)
792_2018_1003_MOESM2_ESM.docx (15 kb)
Supplementary material 2 (DOCX 14 kb)
792_2018_1003_MOESM3_ESM.docx (15 kb)
Supplementary material 3 (DOCX 14 kb)
792_2018_1003_MOESM4_ESM.docx (302 kb)
Supplementary material 4 (DOCX 302 kb)
792_2018_1003_MOESM5_ESM.docx (159 kb)
Supplementary material 5 (DOCX 158 kb)
792_2018_1003_MOESM6_ESM.docx (57 kb)
Supplementary material 6 (DOCX 57 kb)
792_2018_1003_MOESM7_ESM.docx (49 kb)
Supplementary material 7 (DOCX 48 kb)
792_2018_1003_MOESM8_ESM.docx (63 kb)
Supplementary material 8 (DOCX 62 kb)

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amaretti A, Raimondi S, Sala M, Roncaglia L, De Lucia M, Leonardi A, Rossi M (2010) Single cell oils of the cold-adapted oleaginous yeast Rhodotorula glacialis DBVPG 4785. Microb Cell Fact 9:73.  https://doi.org/10.1186/1475-2859-9-73 PubMedPubMedCentralGoogle Scholar
  3. Arenz BE, Held BW, Jurgens JA, Farrell RL, Blanch-ette RA (2006) Fungal diversity in soils and historic wood from the Ross Sea region of Antarctica. Soil Biol Biochem 38:3057–3064.  https://doi.org/10.1016/j.soilbio.2006.01.016 CrossRefGoogle Scholar
  4. Arenz BE, Held BW, Jurgens JA, Blanchette RA (2011) Fungal colonization of exotic substrates in Antarctica. Fungal Divers 49:13–22.  https://doi.org/10.1007/s13225-010-0079-4 CrossRefGoogle Scholar
  5. Baschien C, Tsui CKM, Gulis V, Szewzyk U, Marvanov L (2013) The molecular phylogeny of aquatic hyphomycetes with affinity to the Leotiomycetes. Fungal Biol 117:660–672.  https://doi.org/10.1016/j.funbio.2013.07.004 CrossRefPubMedGoogle Scholar
  6. Baublis JA, Wharton RA, Volz PA (1991) Diversity of micro-fungi in an Antarctic dry valley. J Basic Microbiol 31:3–12.  https://doi.org/10.1002/jobm.3620310102 CrossRefPubMedGoogle Scholar
  7. Boerema GH, von Arx JA (1964) Ein neuer zur Gattung Ingoldia geh€orender Pilz. Nova Hedwigia 8:297–300.  https://doi.org/10.1126/science.1163874 Google Scholar
  8. Bridge PD, Newsham KK (2009) Soil fungal community composition at Mars Oasis, a southern maritime Antarctic site, assessed by PCR amplification and cloning. Fungal Ecol 2:66–74.  https://doi.org/10.1016/j.funeco.2008.10.008 CrossRefGoogle Scholar
  9. Brunati M, Rojas JL, Sponga F, Ciciliato I, Losi D, Göttlich E, de Hoog S, Genilloud O, Marinelli F (2009) Diversity and pharmaceutical screening of fungi from benthic mats of Antarctic lakes. Mar Genom 2:43–50.  https://doi.org/10.1016/j.margen.2009.04.002 CrossRefGoogle Scholar
  10. Callahan HL, Portal AC, Devereaux R, Grogl M (1997) An axenic amastigote system for drug screening. Antimicrob Agents Chemother 41:818–822PubMedPubMedCentralGoogle Scholar
  11. Dayan FE, Romagni JG, Duke SO (2000) Investigating the mode of action of natural phytotoxins. J Chem Ecol 26:2079–2094.  https://doi.org/10.1023/A:1005512331061 CrossRefGoogle Scholar
  12. De García V, Brizzio S, Libkind D, Buzzini P, Broock MV (2007) Biodiversity of cold-adapted easts from glacial meltwater rivers in Patagonia Argentina. FEMS Microbiol Ecol 59:331–341.  https://doi.org/10.1111/j.1574-6941.2006.00239.x CrossRefPubMedGoogle Scholar
  13. Defelipo BV, Ribeiro AC (1981) Análise química de solos (metodologia). Viçosa, BrasilGoogle Scholar
  14. di Menna ME (1966) Yeasts in Antarctic soils. Antonie Van Leeuwenhoek 32:29–38.  https://doi.org/10.1007/BF02097443 CrossRefPubMedGoogle Scholar
  15. EMBRAPA (1997) Manual de métodos de análise de solo. EMBRAPA-CNPS, BrasilGoogle Scholar
  16. Flores MG, Rodríguez ME, Oteiza JM, Barbagelata RJ, Lopes CA (2017) Physiological characterization of Saccharomyces uvarum and Saccharomyces eubayanus from Patagonia and their potential for cidermaking. Int J Food Microbiol 249:9–17.  https://doi.org/10.1016/j.ijfoodmicro.2017.02.018 CrossRefGoogle Scholar
  17. Francelino MR, Schaefer CEGR, Simas FNB, Filho EIF, Souza JJLL, Costa LM (2011) Geomorphology and soils distribution under paraglacial conditions in an ice-free area of Admiralty Bay, King George Island, Antarctica. CATENA 85:194–204.  https://doi.org/10.1016/j.catena.2010.12.007 CrossRefGoogle Scholar
  18. Francesca N, Canale DE, Settanni L, Moschetti G (2012) Dissemination of wine-related yeasts by migratory birds. Environ Microbiol Rep 4:105–112.  https://doi.org/10.1111/j.1758-2229.2011.00310 CrossRefPubMedGoogle Scholar
  19. Furbino LE, Godinho VM, Santiago IF, Pellizari FM, Alves TMA, Zani CL, Junior AS, Romanha AJ, Carvalho AGO, Gil LHVG, Rosa CA, Minnis AM, Rosa LH (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microb Ecol 67:775–787.  https://doi.org/10.1007/s00248-014-0374-9 CrossRefPubMedGoogle Scholar
  20. 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 61:1323–1330PubMedPubMedCentralGoogle Scholar
  21. Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya N, Pupo D, Alves TMA, Junior PAS, Romanha AJ, Zani CL, Cantrell C, Rosa CA, Rosa LH (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J7:1434–1451.  https://doi.org/10.1038/ismej.2013.77 CrossRefGoogle Scholar
  22. Godinho VM, Gonçalves VN, Santiago IF, Figueredo HM, Vitoreli GA, Schaefer CEGR, Barbosa EC, Oliveira JG, Alves TMA, Zani CL, Junior PAS, Murta SMF, Romanha AJ, Kroon EG, Cantrell CL, Wedge DE, Duke SO, Ali A, Rosa CA, Rosa LH (2015) Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 19:585–596.  https://doi.org/10.1007/s00792-015-0741-6 CrossRefPubMedGoogle Scholar
  23. 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.  https://doi.org/10.1111/j.1574-6941.2012.01424.x CrossRefPubMedGoogle Scholar
  24. Gonçalves VN, Cantrell CL, Wedge DE, Ferreira MC, Soares MA, Jacob MR, Oliveira FS, Galante D, Rodrigues F, Alves TMA, Zani CL, Junior PAS, Murta S, Romanha AJ, Barbosa EC, Kroon EG, Oliveira JG, Gomez-Silva B, Galetovic A, Rosa CA, Rosa LH (2015) Fungi associated with rocks of the Atacama Desert: taxonomy, distribution, diversity, ecology and bioprospection for bioactive compounds. Environ Microbiol 18:232–245.  https://doi.org/10.1111/1462-2920.13005 CrossRefPubMedGoogle Scholar
  25. Gonçalves VN, Oliveira FS, Carvalho C, Schaefer CEG, Rosa CA, Rosa LH (2017) Antarctic rocks from continental Antarctica as source of potential human opportunistic fungi. Extremophiles 21:851–860.  https://doi.org/10.1007/s00792-017-0947-x CrossRefPubMedGoogle Scholar
  26. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  27. Hou CT (2008) New bioactive fatty acids. Asia Pac J Clin Nutr 17(S1):192–195PubMedGoogle Scholar
  28. Houbraken J, Frisvad JC, Seifert KA, Overy DP, Tuthill DM, Valdez JG, Samson RA (2012) New penicillin-producing Penicillium species and an overview of section Chrysogena. Persoonia 29:78–100.  https://doi.org/10.3767/003158512X660571 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi. CAB International, WallingfordGoogle Scholar
  30. Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study. Elsevier, AmsterdamGoogle Scholar
  31. Lachance MA, Bowles JM, Starmer WT, Barker JSF (1999) Kodamaea kakaduensis and Candida tolerans, two new yeast species from Australian Hibiscus flowers. Can J Microbiol 45:172–177CrossRefPubMedGoogle Scholar
  32. Langwig KE, Frick WF, Reynolds R, Parise KL, Drees KP, Hoyt JR, Cheng TL, Kunz TH, Foster JT, Kilpatric AM (2015) Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc R Soc B 282:20142335.  https://doi.org/10.1098/rspb.2014.2335 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Li Y, Sun B, Liu S, Jiang L, Liu X, Zhang H, Che Y (2008) Bioactive asterric acid derivatives from the Antarctic ascomycete fungus Geomyces sp. J Nat Prod 71:1643–1646.  https://doi.org/10.1021/np8003003 CrossRefPubMedGoogle Scholar
  34. Libkind D, Hittinger CT, Valerio E, Gonçalves C, Diver J, Johnston M, Gonçalves P, Sampaio JP (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. PNAS 108:1–6.  https://doi.org/10.1073/pnas.1105430108 CrossRefGoogle Scholar
  35. Lopes DV, Souza JJLL, Oliveira FS, Schaefer CEGR (2017) Solos e Evolução da Paisagem em Ambiente Periglacial na Península Barton, Antártica Marítima. Revista do Departamento de Geografia da USP 17:259–267.  https://doi.org/10.11606/rdg.v0ispe.132721 Google Scholar
  36. 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.  https://doi.org/10.1007/s00300-009-0740-0 CrossRefGoogle Scholar
  37. Lorch JM, Meteyer CU, Behr JM, Boyles JG, Cryan PM, Hicks AC, Ballmann AE, Coleman JTH, Redell DN, Reeder DM, Blehert DS (2011) Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480:376–378.  https://doi.org/10.1038/nature10590 CrossRefPubMedGoogle Scholar
  38. 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.  https://doi.org/10.3852/12-207 CrossRefPubMedGoogle Scholar
  39. Margesin R, Fonteyne PA, Schinner F, Sampaio JP (2007) Rhodotorula psychrophila sp. nov., Rhodotorula psychrophenolica sp. nov. and Rhodotorula glacialis sp. nov., novel psychrophilic basidiomycetous yeast species isolated from alpine environments. Int J Syst Evol Microbiol 57:2179–2184.  https://doi.org/10.1099/ijs.0.65111-0 CrossRefPubMedGoogle Scholar
  40. McRae CF, Hocking AD, Seppelt RD (1999) Penicillium species from terrestrial habitats in the Windmill Islands, East Antarctica, including a new species, Penicillium antarcticum. Polar Biol 21:97–111.  https://doi.org/10.1007/s003000050340 CrossRefGoogle Scholar
  41. Melo IS, Santos SN, Rosa LH, Parma MM, Silva LJ, Queiroz SCN, Pellizari VH (2014) Isolation and biological activities of an endophytic Mortierella alpina strain from the Antarctic moss Schistidium antarctici. Extremophiles 18:15–23CrossRefPubMedGoogle Scholar
  42. Mercantini R, Marsellan R, Cervellati C (1989) Keratinophilic fungi isolated from antarctic soil. Mycopathologia 106:47–52.  https://doi.org/10.1007/s00792-013-0588-7 CrossRefPubMedGoogle Scholar
  43. 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.  https://doi.org/10.1016/j.funbio.2013.07.001 CrossRefPubMedGoogle Scholar
  44. Mossman T (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55–63CrossRefGoogle Scholar
  45. Pathan AAK, Bhadra B, Begum Z, Shivaji S (2010) Diversity of yeasts from puddles in the vicinity of Midre Lovénbreen glacier, Arctic and bioprospecting for enzymes and fatty acids. Current Microbiol 60:307–314.  https://doi.org/10.1007/s00284-009-9543-3 CrossRefPubMedGoogle Scholar
  46. Pereira TTC, Schaefer CEGR, Ker JC, Almeida CC, Almeida ICC (2013) Micromorphological and microchemical indicators of pedogenesis in ornithogenic cryosols (gelisols) of Hope Bay, Antartic Peninsula. Geoderma 193:311–322.  https://doi.org/10.1016/j.geoderma.2012.10.023 CrossRefGoogle Scholar
  47. Rodríguez ME, Pérez-Través L, Sangorrín MP, Barrio E, Lopes CA (2014) Saccharomyces eubayanus and Saccharomyces uvarum associated with the fermentation of Araucaria araucana seeds in Patagonia. FEMS Yeast Res 14:948–965.  https://doi.org/10.1111/1567-1364.12183 CrossRefPubMedGoogle Scholar
  48. Romanha AJ, de Castro SL, Soeiro MNC, Lannes-Vieira J, Ribeiro I, Talvani A, Bourdin B, Blum B, Olivieri B, Zani C, Spadafora C, Chiari E, Chatelain E, Chaves G, Calzada JE, Bustamante JM, Freitas-Junior LH, Romero LI, Bahia MT, Lotrowska M, Soares M, Andrade SG, Armstrong T, Degrave W, Andrade Zde A (2010) In vitro and in vivo experimental models for drug screening and development for Chagas disease. Mem Inst Oswaldo Cruz 105:233–238.  https://doi.org/10.1590/S0074-02762010000200022 CrossRefPubMedGoogle Scholar
  49. 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.  https://doi.org/10.1007/s00300-008-0515-z CrossRefGoogle Scholar
  50. 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.  https://doi.org/10.1111/j.1574-6941.2010.00872.x PubMedGoogle Scholar
  51. Rosa LH, Queiroz SCN, Moraes RM, Wang X, Techen N, Pan Z, Cantrell CL, Wedge DE (2013) Coniochaeta ligniaria: antifungal activity of the cryptic endophytic fungus associated with autotrophic tissue cultures of the medicinal plant Smallanthus sonchifolius (Asteraceae). Symbiosis 60:133–142.  https://doi.org/10.1007/s13199-013-0249-8 CrossRefGoogle Scholar
  52. Rudolph ED (1970) Local dissemination of plant propagules in Antarctica. In: Holdgate MW (ed) Antarctic Ecology, vol 2. Academic Press, LondonGoogle Scholar
  53. Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141.  https://doi.org/10.1007/s11157-006-9107-y CrossRefGoogle Scholar
  54. Sampaio JP, Kirschner R, Oberwinkler F (2011a) Rhodotorula Harrison (1928). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. 5th edn, Elsevier, Amsterdam, pp 1873–1927CrossRefGoogle Scholar
  55. Santiago IF, Alves TM, Rabello A, Junior PAS, Romanha AJ, Zani CL, Rosa CA, Rosa LH (2012) Leishmanicidal and antitumoral activities of endophytic fungi associated with the Antarctic angiosperms Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. Extremophiles 16:95–103.  https://doi.org/10.1007/s00792-011-0409-9 CrossRefPubMedGoogle Scholar
  56. Santiago IF, Soares MA, Rosa CA, Rosa LH (2015) Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19:1087–1097.  https://doi.org/10.1007/s00792-015-0781-y CrossRefPubMedGoogle Scholar
  57. Santiago IF, Rosa CA, Rosa LH (2016) Endophytic symbiont yeasts associated with the Antarctic angiosperms Deschampsia antarctica and Colobanthus quitensis. Polar Biol 40:177–183.  https://doi.org/10.1007/s00300-016-1940-z CrossRefGoogle Scholar
  58. Schaefer CEGR, Simas FNB, Filho MRA, Michel RFM, Viana JHM, Tatur A (2004) Fosfatização: processo de formação de solos na Baía do Almirantado e implicações ambientais. In: Schaefer CEGR, Francelino R, Simas FNB, Filho RA (eds) Ecossistemas costeiros e monitoramento ambiental da Antártica Marítima, Baía do Almirantado, Ilha Rei George. NEPUT e Departamento de Solos, Viçosa, pp 47–59Google Scholar
  59. Simas FNB, Schaefer CEGR, Melo VF, Filho MRA, Michel RFM, Pereira VV, Gomes MRM, Costa LM (2007) Ornithogenic cryosols from Maritime Antarctica: phosphatization as a soil forming process. Geoderma 138:191–203.  https://doi.org/10.1016/j.geoderma.2006.11.011 CrossRefGoogle Scholar
  60. Simas FNB, Schaefer CEGR, Filho MRA, Francelino MR, Fernandes Filho EI, Costa LM (2008) Genesis, properties and classification of cryosols from Admiralty Bay, Maritime Antarctica. Geoderma 144:116–122.  https://doi.org/10.1016/j.geoderma.2007.10.019 CrossRefGoogle Scholar
  61. Singh P, Singh SM (2012) Characterization of yeast and filamentous fungi isolated from cryoconite holes of Svalbard, Arctic. Polar Biol 35:575–583.  https://doi.org/10.1007/s00300-011-1103-1 CrossRefGoogle Scholar
  62. Souza KKD, Schaefer CEGR, Simas FNB, Spinola DN, De Paula MD (2014) Soil formation in Seymour Island, Weddell Sea, Antarctica. Geomorphology 225:87–99.  https://doi.org/10.1016/j.geomorph.2014.03.047 CrossRefGoogle Scholar
  63. Sugiyama J, Sugiyama Y, Iizuka H (1967) Report of the Japanese summer parties in Dry Valleys, Victoria Land, 1963-1965. III. Mycological Studies of the Antarctic Fungi. Part 1. Historical. Antarctic Record 28:15–22Google Scholar
  64. Suji M, Fujiu S, Xiao N, Hanada Y, Kudoh S, Kondo H, Tsuda S, Hoshino T (2013) Cold adaptation of fungi obtained from soil and lake sediment in the Skarvsnes ice-free area, Antarctica. FEMS Microbiol Lett 346:121–130.  https://doi.org/10.1111/1574-6968.12217 CrossRefGoogle Scholar
  65. 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.  https://doi.org/10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Tatur A (1989) Ornithogenic soils of the maritime antarctic. Polish Pol Res 4:481–532Google Scholar
  67. Tatur A, Barczuk A (1985) Ornithogenic phosphates on King George Island, Maritime Antarctic. In: Siegfried WR, Condy PR, Laws RM (eds), Antarctic nutrient cycles and food webs. Springer, New York, pp 63–169.  https://doi.org/10.1007/978-3-642-82275-9
  68. Tatur A, Myrcha A (1984) Ornithogenic soils on King George Island (maritime Antarctic zone). Polish Pol Res 5:31–60Google Scholar
  69. Thomas-Hall SR, Turchetti B, Buzzini P, Branda E, Boekhout T, Threelen B, Watson K (2010) Cold-adapted yeasts from Antarctica and Italian Alps-description of three novel species: Mrakia robertii sp. nov., Mrakiablollopis sp.nov. and Mrakiella niccombsii sp. nov. Extremophiles 14:47–59.  https://doi.org/10.1007/s00792-009-0286-7 CrossRefPubMedGoogle Scholar
  70. Tosi S, Casado B, Gerdol R (2002) Fungi isolated from Antarctic mosses. Polar Biol 25:262–268.  https://doi.org/10.1007/s00300-001-0337-8 Google Scholar
  71. Tsuji M (2016) Cold-stress responses in the Antarctic basidiomycetous yeast Mrakia blollopis. R Soc Open Sci 3:160106.  https://doi.org/10.1098/rsos.160106 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Vaz ABM, Rosa LH, Vieira MLA, Garcia V, Brandão LR, Teixeira LCRS, MolinéII M, LibkindII D, BroockII MV, Rosa CA (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Br J Microbiol 42:937–947.  https://doi.org/10.1590/S1517-838220110003000012 CrossRefGoogle Scholar
  73. Vishniac HS (2017) A multivariate analysis of soil yeasts isolated from a latitudinal gradient. Microbial Ecol 52:90–103.  https://doi.org/10.1007/s00248-006-9066-4 CrossRefGoogle Scholar
  74. Wang QM, Yurkov AM, Göker M, Lumbsch HT, Leavitt SD, Groenewald M, Theelen B, Liu X-Z, Boekhout T, Bai F-Y (2016) Phylogenetic classification of yeasts and related taxa within Pucciniomycotina. Stud Mycol 81:149–189.  https://doi.org/10.1016/j.simyco.2015.12.002 CrossRefPubMedCentralGoogle Scholar
  75. 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, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  76. Zucconi L, Selbmann L, Buzzini P, Turchetti B, Guglielmin M, Frisvad JC, Onofri S (2012) Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol 35:749–757.  https://doi.org/10.1007/s00300-011-1119-6 CrossRefGoogle Scholar
  77. Zukal J, Bandouchova H, Brichta J, Cmokova A, Jaron KS, Kolarik M, Kovacova V, Kubátová A, Nováková A, Orlov O, Pikula J, Presetnik P, Šuba J, Zahradníková AJ, Martínková N (2016) White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Rep 6:19829.  https://doi.org/10.1038/srep19829 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Eldon C. Q. Gomes
    • 1
  • Valéria M. Godinho
    • 1
  • Débora A. S. Silva
    • 1
  • Maria T. R. de Paula
    • 1
  • Gislaine A. Vitoreli
    • 1
  • Carlos L. Zani
    • 2
  • Tânia M. A. Alves
    • 2
  • Policarpo A. S. Junior
    • 2
  • Silvane M. F. Murta
    • 2
  • Emerson C. Barbosa
    • 2
  • Jaquelline G. Oliveira
    • 2
  • Fabio S. Oliveira
    • 3
  • Camila R. Carvalho
    • 1
  • Mariana C. Ferreira
    • 1
  • Carlos A. Rosa
    • 1
  • Luiz H. Rosa
    • 1
  1. 1.Department of MicrobiologyFederal University of Minas GeraisBelo HorizonteBrazil
  2. 2.Centro de Pesquisas René RachouFIOCRUZ-MGBelo HorizonteBrazil
  3. 3.Department of GeographyFederal University of Minas GeraisBelo HorizonteBrazil

Personalised recommendations