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Diversity and ecology of cultivable fungi isolated from the thermal soil gradients in Deception Island, Antarctica

  • Hebert M. Figueredo
  • Vívian N. Gonçalves
  • Valéria M. Godinho
  • Daví V. Lopes
  • Fabio S. Oliveira
  • Luiz H. RosaEmail author
Original Paper
  • 40 Downloads

Abstract

We surveyed the diversity of cultivable fungi isolated from cold and hot volcanic soils of Deception Island, Antarctica. Seventy-four fungal isolates were identified; these belonged to 17 taxa in the genera Aspergillus, Penicillium, Pseudogymnoascus, Purpureocillium, and Mortierella. The fungal assemblages showed low diversity, richness, and dominance indices. The Aspergillus taxa were dominant in the soils at 0 °C, 50 °C, and 100 °C. Aspergillus lacticoffeatus, Aspergillus cf. ruber, Penicillium citrinun, and Purpureocillium sodanum were present only in soils having a temperature of 100 °C. Aspergillus calidoustus was present in all thermal soils and displayed the highest densities. The majority of fungi displayed mesophilic behavior; however, different isolates of Aspergillus lacticoffeatus and Aspergillus niger were able to grow at 50 °C; these are phylogenetically close to the causative agents of aspergillosis in immunocompromised individuals. Deception Island perhaps represents one of the most visited regions in Antarctica and the tourism there has increased over the last 20 years, especially by elderly tourists, probably with weak immune systems, come in contact with the resident microorganisms, including the thermo-resistant opportunistic Aspergillus species.

Keywords

Antarctica Aspergillus Fungi Opportunistic fungi Psychrophilic Thermophilic 

Notes

Acknowledgements

We acknowledge the financial support from CNPq PROANTAR 442258/2018-6, INCT Criosfera II, CAPES (88887.136384/2017-00 and 88887.314457/2019-00), CNPq, FAPEMIG, and FNDCT.

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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. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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 43:308–315CrossRefGoogle Scholar
  3. Azmi OR, Seppelt RD (1998) Fungi of the Windmill Islands, continental Antarctica. Effect of temperature, pH and culture media on the growth of selected microfungi. Polar Biol 18:128–134CrossRefGoogle Scholar
  4. Bardou P, Mariette J, Escudié F et al (2014) An interactive Venn diagram viewer. BMC Bioinformatics 15:293PubMedPubMedCentralCrossRefGoogle Scholar
  5. Blöchl E, Rachel R, Burggraf S, Hafenbradl D, Jannasch HW, Stetter KO (1997) Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113°C. Extremophiles 1:14–21PubMedCrossRefGoogle Scholar
  6. 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 2:66–74CrossRefGoogle Scholar
  7. Brock TD (1995) The road to Yellowstone and beyond. Annu Rev Microbiol 49:1–28PubMedCrossRefGoogle Scholar
  8. Cooney DG, Emerson R (1964) Thermophilic fungi: an account of their biology, activities and classification. W.H. Freeman & Co., San FranciscoGoogle Scholar
  9. Crisan EV (1973) Current concepts of thermophilism and the thermophilic fungi. Mycologia 65:1171–1198PubMedCrossRefGoogle Scholar
  10. Ellis DH (1980) Thermophilic fungi isolated from a heated aquatic habitat. Mycologia 72:1030–1033CrossRefGoogle Scholar
  11. Fell JW, Scorzetti G, Connell L, Craig S (2006) Biodiversity of micro-eukaryotes in Antarctic Dry Valley soils with %3c 5% soil moisture. Soil Biol Biochem 38:3107–3119CrossRefGoogle Scholar
  12. Furbino LE, Godinho VM, Santiago IF et al (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic. Microbial Ecol 67:775–787CrossRefGoogle Scholar
  13. Gautier M, Normand AC, Ranque S (2016) Previously unknown species of Aspergillus. Clin Microbiol Infect 22:662–669PubMedCrossRefGoogle Scholar
  14. 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
  15. Godinho VM, Furbino LE, Santiago IF et al (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451PubMedPubMedCentralCrossRefGoogle Scholar
  16. Godinho VM, Gonçalves VN, Santiago IF, Figueredo HM, Vitoreli GA, Schaefer CEGR et al (2015) Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 19:585–596PubMedCrossRefGoogle Scholar
  17. Gomes EC, Godinho VM, Silva DA et al (2018) Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites. Extremophiles 22:381–393PubMedCrossRefPubMedCentralGoogle Scholar
  18. Gonçalves VN, Vaz ABM, Rosa CA et al (2012) Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol Ecol 82:459–471PubMedCrossRefPubMedCentralGoogle Scholar
  19. Gonçalves VN, Carvalho CR, Susana Johann S et al (2015) Antibacterial, antifungal and antiprotozoal activities of fungal communities present in different substrates from Antarctica. Polar Biol 38:1143–1152CrossRefGoogle Scholar
  20. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Paleont Electron 4:1–9Google Scholar
  21. 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 29:78–100PubMedPubMedCentralCrossRefGoogle Scholar
  22. Houbraken J, de Vries RP, Samson RA (2014) Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. In: San AAM (ed) Sariaslani S, Gadd GM. Academic Press, Diego, pp 199–249Google Scholar
  23. Jesenská Z, Piecková E, Bernát D (1993) Heat resistance of fungi from soil. Int J Food Microbiol 19:187–192PubMedCrossRefGoogle Scholar
  24. Kane BE, Mullins JT (1973) Thermophilic fungi in a municipal waste compost system. Mycologia 65:1087–1100PubMedCrossRefGoogle Scholar
  25. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. Wallingford, UK, CAB InternationalGoogle Scholar
  26. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549PubMedPubMedCentralCrossRefGoogle Scholar
  27. Loque CP, Medeiros AO, Pellizzari FM, Oliveira EC, Rosa CA, Rosa LH (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648CrossRefGoogle Scholar
  28. Madariaga-Mazón A, González-Andrade M, González MC, Glenn AE, Cerda-García-Rojas CM, Mata R (2013) Absolute configuration of acremoxanthone C, a potent calmodulin inhibitor from Purpureocillium lilacinum. J Nat Prod 76:1454–1460PubMedCrossRefGoogle Scholar
  29. Maheshwari R, Bharadwaj G, Bhat MK (2000) Thermophilic fungi: their physiology and enzymes. Microbiol Mol Biol Rev 64:461–488PubMedPubMedCentralCrossRefGoogle Scholar
  30. Munoz PA, Flores PA, Boehmwald FA, Blamey JM (2011) Thermophilic bacteria present in a sample from Fumarole Bay, Deception Island. Antarct Sci 23:549–555CrossRefGoogle Scholar
  31. Oliveira TB, Gomes E, Rodrigues A (2015) Thermophilic fungi in the new age of fungal taxonomy. Extremophiles 19:31–37PubMedCrossRefGoogle Scholar
  32. Pan WZ, Huang XW, Wei KB, Zhang CM, Yang DM, Ding JM, Zhang KG (2010) Diversity of thermophilic fungi in Tengchong Rehai National Park revealed by ITS nucleotide sequence analy-ses. J Microbiol 48:146–152PubMedCrossRefGoogle Scholar
  33. Person AK, Chudgar SM, Norton BL, Tong BC, Stout JE (2010) Aspergillus niger: an unusual cause of invasive pulmonary aspergillosis. J Med Microbiol 59:834–838PubMedPubMedCentralCrossRefGoogle Scholar
  34. Powell AJ, Parchert KJ, Bustamante JM, Ricken JB, Hutchinson MI, Natvig DO (2012) Thermophilic fungi in an aridland ecosystem. Mycologia 104:813–825PubMedCrossRefGoogle Scholar
  35. Rosa LH, Vaz ABM, Caligiorne RB, Campolina S, Rosa CA (2009) Endophytic fungi associated with the Antarctic Grass Deschampsia antarctica Desv. (Poaceae). Polar Biol 32:161–167CrossRefGoogle Scholar
  36. Rosa LH, Vieira MLA, Santiago IF et al (2010) Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol 73:178–189PubMedGoogle Scholar
  37. Rosa LH, Zani CL, Cantrell CL, Duke SO, Van Dijck P, Desideri A, Rosa CA (2019) Fungi in Antarctica: diversity, ecology, effects of climate change, and bioprospection for bioactive compounds. In: Rosa LH (ed) Fungi of Antarctica: diversity, ecology and biotechnological applications. Springer International Publishing, Switzerland, pp 10–17CrossRefGoogle Scholar
  38. Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environm Sci Biotechnol 6:127–141CrossRefGoogle Scholar
  39. Samson RA, Houbraken JAMP, Kuijpers AFA, Frank JM, Frisvad JC (2004) New ochratoxin A or sclerotium producing species in Aspergillus section Nigri. Stud Mycol 50:45–61Google Scholar
  40. Santiago IF, Soares MA, Rosa CA et al (2015) Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19:1087–1097PubMedCrossRefGoogle Scholar
  41. Seroy J, Antiporta P, Grim SA, Proia LA, Singh K, Clark NM (2017) Aspergillus calidoustus case series and review of the literature. Transpl Infect Dis 19:e12755CrossRefGoogle Scholar
  42. Straatsma G, Samson RA, Olijnsma TW, Camp HJM, Gerrits JPG, Griensven LJLD (1994) Ecology of thermophilic fungi in mush-room compost, with emphasis on Scytalidium thermophilum and growth stimulation of Agaricus bisporus mycelium. Appl Environ Microbiol 60:454–458PubMedPubMedCentralGoogle Scholar
  43. Tosi S, Casado B, Gerdol R (2002) Fungi isolated From Antarctic mosses. Polar Biol 25:262–268Google Scholar
  44. Tsang CC, Tang J, Lau S, Woo P (2018) Taxonomy and evolution of Aspergillus, Penicillium and Talaromyces in the omics era—past, present and future. Comput Struct Biotechnol J 16:197–210PubMedPubMedCentralCrossRefGoogle Scholar
  45. Varga J, Houbraken J, Van Der Lee HA, Verweij PE, Samson RA (2008) Aspergillus calidoustus sp. nov., causative agent of human infections previously assigned to Aspergillus ustus. Eukaryot Cell 7:630–638PubMedPubMedCentralCrossRefGoogle Scholar
  46. 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 315–322Google Scholar
  47. 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 35:749–757CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Hebert M. Figueredo
    • 1
  • Vívian N. Gonçalves
    • 1
  • Valéria M. Godinho
    • 1
  • Daví V. Lopes
    • 2
  • Fabio S. Oliveira
    • 2
  • Luiz H. Rosa
    • 1
    Email author
  1. 1.Departamento de MicrobiologiaUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Departamento de GeografiaUniversidade Federal de Minas GeraisBelo HorizonteBrazil

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