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Antarctic Permafrost: An Unexplored Fungal Microhabitat at the Edge of Life

  • Thamar Holanda da Silva
  • Débora Amorim Saraiva Silva
  • André Thomazini
  • Carlos Ernesto Gonçalves Reynaud Schaefer
  • Luiz Henrique Rosa
Chapter

Abstract

The Antarctic continent represents one of the most primal environments in the world. The fungal communities found in this region are complex and have the ability to survive under extreme conditions of dehydration, frequent freeze-thaw cycles, low nutrient concentration, low temperatures, and high exposure to ultraviolet radiation. Current studies on Antarctic fungi are, in its majority, related to soil fungi. However, studies on the fungal community present in permafrost (soils that are permanently frozen for at least 2 consecutive years) are scarce, especially when compared to the number of studies on Arctic permafrost. Therefore, this chapter aims to compile all documented data related to Antarctic permafrost fungi and the importance of permafrost as a substrate that can host a cryptic and unique community of Antarctic fungi. The predominant taxa found in Antarctic permafrost belong to the phylum Ascomycota, followed by taxa belonging to the phyla Basidiomycota,Mortierellomycota, and Mucoromycota. Thus far, 32 families, 45 genera, and 70 species of fungi have been identified in the Antarctic permafrost. Among the 70 fungal species, Cladosporium herbarum has the widest geographic distribution and has been isolated from different regions of Antarctica. Although there are few studies on the fungal diversity in the Antarctic permafrost, this type of frozen soil is of considerable importance to the cold regions of the planet because of the effects of global climate change, especially the potential effect of global warming in the next few years. Microorganisms currently “trapped” in permafrost, possibly in their latent forms, could eventually be dispersed to other regions of the globe. Additionally, undiscovered fungi present in the Antarctic permafrost may represent promising sources of bioproducts for use in biotechnological processes.

Keywords

Antarctica Permafrost Fungi Microorganisms 

References

  1. Andersen NR, Rasmussen PR (1984) The constitution of clerocidin a new antibiotic isolated from Oidiodendron truncatum. Tetrahedron Lett 25:465–468CrossRefGoogle Scholar
  2. Barbosa MAG, Rehn KG, Menezes M, Mariano RDLR (2001) Antagonism of Trichoderma species on Cladosporium herbarum and their enzimatic characterization. Braz J of Microbiol 32:98–104CrossRefGoogle Scholar
  3. Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud in Mycol 72:1–401CrossRefGoogle Scholar
  4. Bockheim JG (1993) Global change and soil formation in the Antarctic region. Joint Russian-American seminar on cryopedology and global change. Russian Academy of Sciences, Russia, In, pp 181–202Google Scholar
  5. Bockheim JG (2015) Cryopedology. Springer, London, p 173Google Scholar
  6. Bockheim JG, Hall KJ (2002) Permafrost, active-layer dynamics and periglacial environments of continental Antarctica: periglacial and permafrost research in the Southern Hemisphere. S Afr J Sci 98:82–90Google Scholar
  7. Bridge PD, Spooner BM (2012) Non-lichenized Antarctic fungi: Transient visitors or members of a cryptic ecosystem? Fungal Ecology 5: 381–394CrossRefGoogle Scholar
  8. Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241CrossRefGoogle Scholar
  9. Czechowski P, Clarke LJ, Breen J, Cooper A, Stevens MI (2016) Antarctic eukaryotic soil diversity of the Prince Charles Mountains revealed by high-throughput sequencing. Soil Biol Biochem 95:112–121CrossRefGoogle Scholar
  10. De Hoog GS, Guarro J, Gene J, Figueras MJ (2000) Atlas of clinical fungi. Centraalbureau voor Schimmelcultures, Utrecht, pp 276–282Google Scholar
  11. Ding Z, Li L, Che Q, Li D, Gu Q, Zhu T (2016) Richness and bioactivity of culturable soil fungi from the Fildes Peninsula, Antarctica. Extremophiles 20:425–435CrossRefGoogle Scholar
  12. Dreborg S, Agrell B, Foucard T, Kjellman NI, Koivikko A, Nillson S (1986) A double-blind, multicenter immunotherapy trial in children, using a purified and standardized Cladosporium herbarum preparation I. clinical results. Allergy 41:131–140CrossRefGoogle Scholar
  13. Dreesens LL, Lee CK, Cary SC (2014) The distribution and identity of edaphic fungi in the McMurdo Dry Valleys. Biol 3:466–483CrossRefGoogle Scholar
  14. Elster J, Margesin R, Wagner D, Häggblom M (2017) Polar and alpine microbiology—earth’s cryobiosphere. FEMS Microbiol Ecol 93:1–3Google Scholar
  15. 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 85:194–204CrossRefGoogle Scholar
  16. Gilichinsky D, Rivkina E, Shcherbakova V, Laurinavichuis K, Tiedje J (2003) Supercooled water brines within permafrost-an unknown ecological niche for microorganisms: a model for astrobiology. Astrobiology 3:331–341CrossRefGoogle Scholar
  17. Gilichinsky DA, Wilson GS, Friedmann EI, McKay CP, Sletten RS, Rivkina EM, Vishnivetskaya TA, Erokhina LG, Ivanushkina NE, Kochkina GA, Shcherbakova VA, Soina VS, Spirina EV, Vorobyova EA, Fyodorov-Davydov DG, Hallet B, Ozerskaya SM, Sorokovikov VA, Laurinavichyus KS, Shatilovich AV, Chanton JP, Ostroumov VE, Tiedje JM (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology 7:275–311CrossRefGoogle Scholar
  18. Gomes EC, Godinho VM, Silva DA, de Paula MT, Vitoreli GA, Zani CL, Alves TMA, Junior PAS, Furta SMF, Barbosa EC, Oliveira JG, Oliveira FS, Carvalho CR, Ferreira MC, Rosa CA, Rosa LH (2018) Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites. Extremophiles 22:381–393CrossRefGoogle Scholar
  19. Goordial J, Davila A, Lacelle D, Pollard W, Marinova MM, Greer CW, DiRuggiero J, McKay CP, Whyte LG (2016) Nearing the cold-arid limits of microbial life in permafrost of an upper Dry Valley, Antarctica. ISME J 10:1613CrossRefGoogle Scholar
  20. Goordial J, Davila A, Greer CW, Cannam R, DiRuggiero J, McKay CP, Whyte LG (2017) Comparative activity and functional ecology of permafrost soils and lithic niches in a hyper-arid polar desert. Environ Microbiol 19:443–458CrossRefGoogle Scholar
  21. Guglielmin M, Cannone N (2012) A permafrost warming in a cooling Antarctica? Clim Chang 111:177–195CrossRefGoogle Scholar
  22. Hultman J, Waldrop MP, Mackelprang R, David MM, McFarland J, Blazewicz SJ, Harden J, Turetsky MR, McGuire AD, Shah MB, VerBerkmoes NC, Lee LH, Mavrommatis K, Jansson JK (2015) Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521:208CrossRefGoogle Scholar
  23. Jansson JK, Taş N (2014) The microbial ecology of permafrost. Nat Rev Microbiol 12:414CrossRefGoogle Scholar
  24. Kerfoot DE (1972) Thermal contraction cracks in an Arctic tundra environment. Arctic 25:142–150CrossRefGoogle Scholar
  25. Kochkina GA, Ivanushkina NE, Karasev SG, Gavrish EY, Gurina LV, Evtushenko LI, Spirina EV, Vorob’eva EA, Gilichinskii DA, Ozerskaya SM (2001) Survival of micromycetes and actinobacteria under conditions of long-term natural cryopreservation. Microbiology 70:356–364CrossRefGoogle Scholar
  26. Kochkina G, Ivanushkina N, Ozerskaya S, Chigineva N, Vasilenko O, Firsov S, Spirina E, Gilichinsky D (2012) Ancient fungi in Antarctic permafrost environments. FEMS Microbiol Ecol 82:501–509CrossRefGoogle Scholar
  27. Kochkina GA, Ozerskaya SM, Ivanushkina NE, Chigineva NI, Vasilenko OV, Spirina EV, Gilichinskii DA (2014) Fungal diversity in the Antarctic active layer. Microbiology 83:94–101CrossRefGoogle Scholar
  28. Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, Lescot M, Poirot O, Bertaux L, Bruley C, Couté Y, Rivkina E, Abergel C, Claverie J-M (2014) Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc Natl Acad Sci 111:4274–4279CrossRefGoogle Scholar
  29. Li L, Li D, Luan Y, Gu Q, Zhu T (2012) Cytotoxic metabolites from the Antarctic psychrophilic fungus Oidiodendron truncatum. J Nat Prod 75:920–927CrossRefGoogle Scholar
  30. 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
  31. Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ, Jansson JK (2011) Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature, 480:368CrossRefGoogle Scholar
  32. Malling HJ, Dreborg S, Weeke B (1986) Diagnosis and immunotherapy of mould allergy: V. clinical efficacy and side effects of immunotherapy with Cladosporium herbarum. Allergy 41:507–519CrossRefGoogle Scholar
  33. Maxwell JB, Barrie LA (1989) Atmospheric and climatic change in the Arctic and Antarctic. Ambio 18:42–49Google Scholar
  34. Michel RFM, Schaefer CEGR, Dias L, Simas FNB, Benites V, Mendonca ES (2006) Ornithogenic gelisols (cryosols) from Maritime Antarctica: pedogenesis, vegetation and carbon studies. Soil Sci Soc Am J 70:1370–1376CrossRefGoogle Scholar
  35. Michel RFM, Schaefer CEGR, Poelking EL, Simas FNB, Fernandes Filho EI, Bockheim JG (2012) Active layer temperature in two Cryosols from King George Island, Maritime Antarctica. Geomorphology 155:12–19CrossRefGoogle Scholar
  36. Mondav R, Woodcroft BJ, Kim EH, McCalley CK, Hodgkins SB, Crill PM, Chanton J, Hurst GB, VerBerkmoes NC, Saleska SR, Hugenholtz P, Rich VI, Tyson GW (2014) Discovery of a novel methanogen prevalent in thawing permafrost. Nat Commun 5:3212CrossRefGoogle Scholar
  37. Moura PA, Francelino MR, Schaefer CEGR, Simas FNB, Mendonça BAF (2012) Distribution and characterization of soils and landform relationships in Byers Peninsula, Livingston Island, Maritime Antarctica. Geomorphology 155–156:45–54CrossRefGoogle Scholar
  38. Nikrad MP, Kerkhof LJ, Häggblom MM (2016) The subzero microbiome: microbial activity in frozen and thawing soils. FEMS Microbiol Ecol 92:fiw081CrossRefGoogle Scholar
  39. Ozerskaya S, Kochkina G, Ivanushkina N, Gilichinsky DA (2009) Fungi in permafrost. In: Permafrost soils. Springer, Berlin, Heidelberg, pp 85–95CrossRefGoogle Scholar
  40. Ramos M, Vieira G, de Pablo MA, Molina A, Abramov A, Goyanes G (2017) Recent shallowing of the thaw depth at Crater Lake, Deception Island, Antarctica (2006–2014). Catena 149:519–528CrossRefGoogle Scholar
  41. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353CrossRefGoogle Scholar
  42. Schubert K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M, Hill CF, Zalar P, de Hoog GS, Crous PW (2007) Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Stud Mycol 58:105–156CrossRefGoogle Scholar
  43. Schuur E, Mcguire A, Scha¨del C, Grosse G, Harden JW, Hayes DJ, Hugelius G, Koven CD, Kuhry P, Lawrence DM, Natali SM, Olefeldt D, Romanovsky VE, Schaefer K, Turetsky MR, Treat CC, Vonk JE (2015) Climate change and the permafrost carbon feedback. Nature 520:171–179CrossRefGoogle Scholar
  44. Selbmann L, Isola D, Fenice M, Zucconi L, Sterflinger K, Onofri S (2012) Potential extinction of Antarctic endemic fungal species as a consequence of global warming. Sci Total Environ 438:127–134CrossRefGoogle Scholar
  45. Shur YL, Jorgenson MT (2007) Patterns of permafrost formation and degradation in relation to climate and ecosystems. Permafrost Periglac 18:7–19CrossRefGoogle Scholar
  46. Simas FNB, Schaefer CEGR, Albuquerque Filho MR, Francelino MR, Fernandes Filho EI, Costa LM (2007) Genesis, properties and classification of Cryosols from Admiralty Bay, Maritime Antarctica. Geoderma 144:116–122CrossRefGoogle Scholar
  47. Solomon S (1999) Stratospheric ozone depletion: a review of concepts and history. Rev Geophys 37:275–316CrossRefGoogle Scholar
  48. Steven B, Leveille R, Pollard WH, Whyte LG (2006) Microbial ecology and biodiversity in permafrost. Extremophiles 10:259–267CrossRefGoogle Scholar
  49. Tarnocai C (1980) Summer temperatures of cryosolic soils in the north-central Keewatin, NWT. Can J Soil Sci 60:311–327CrossRefGoogle Scholar
  50. Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochem Cycles 23CrossRefGoogle Scholar
  51. Thomazini A, Teixeira DB, Turbay CVG, La Scala N, Schaefer CEGR, Mendonça ES (2014) Spatial variability of CO2 emissions from newly exposed paraglacial soils at a glacier retreat zone on King George Island, Maritime Antarctica. Permafrost Periglac 25:233–242CrossRefGoogle Scholar
  52. Thomazini A, Mendonça ES, Teixeira DB, ICC A, La Scala N, Canellas LP, Spokas KA, DMBP M, CVG T, RBA F, CEGR S (2015) CO2 and N2O emissions in a soil chronosequence at a glacier retreat zone in Maritime Antarctica. Sci Total Environ 521-522:336–345CrossRefGoogle Scholar
  53. Thomazini A, Francelino MR, Pereira AB, Schünemann AL, Mendonça ES, Almeida PHA, Schaefer CEGR (2016) Science of the total environment geospatial variability of soil CO2 –C exchange in the main terrestrial ecosystems of Keller Peninsula, Maritime Antarctica. Sci Total Environ 562:802–811CrossRefGoogle Scholar
  54. Vieira G, Bockheim J, Guglielmin M, Balks M, Abramov AA, Boelhouwers J, Cannone N, Ganzert L, Gilichinsky DA, Goryachkin S, López-Martínez J, Meiklejohn, Raffi R, Miguel Ramos SC, Serrano E, Simas F, Sletten R, Wagner D (2010) Thermal state of permafrost and active-layer monitoring in the Antarctic: advances during the international polar year 2007–2009. Permafrost Periglac 21:182–197CrossRefGoogle Scholar
  55. Vonk JE, Mann PJ, Dowdy KL, Davydova A, Davydov SP, Zimoc N, Spencer RGM, Bulygina EB, Eglinton TI, Holmes RM (2013) Dissolved organic carbon loss from Yedoma permafrost amplified by ice wedge thaw. Environ Res Lett 8:035023CrossRefGoogle Scholar
  56. Vorobyova E, Soina V, Gorlenko M, Minkovskaya N, Zalinova N, Mamukelashvili A, Gilichinsky D, Rivkina E, Vishnivetskaya T (1997) The deep cold biosphere: facts and hypothesis. FEMS Microbiol Rev 20:277–290CrossRefGoogle Scholar
  57. Vorobyova E, Minkovsky N, Mamukelashvili A, Zvyagintsev D, Soina V, Polanskaya L, Gilichinsky D (2001) Micro-organisms and biomarkers in permafrost. In: Permafrost response on economic development, environmental security and natural resources. Springer, Dordrecht, pp 527–541CrossRefGoogle Scholar
  58. Wentzel LCP, Inforsato FJ, Montoya QV, Rossin BG, Nascimento NR, Rodrigues A, Sette LD (2018) Fungi from Admiralty Bay (King George Island, Antarctica) soils and marine sediments. Microb Ecol 77:12–24CrossRefGoogle Scholar
  59. Willerslev E, Hansen AJ, Poinar HN (2004) Isolation of nucleic acids and cultures from fossil ice and permafrost. Trends Ecol Evol 19:141–147CrossRefGoogle Scholar
  60. Yano S, Koyabashi K, Kato K (2003) Intrabronchial lesion due to Cladosporium sphaerospermum in a healthy, non-asthmatic woman. Mycoses 46:330–332CrossRefGoogle Scholar
  61. Zhelifonova VP, Antipova TV, Ozerskaya SM, Kochkina GA, Kozlovsky AG (2009) Secondary metabolites of Penicillium fungi isolated from permafrost deposits as chemotaxonomic markers. Microbiology 78:350–354CrossRefGoogle Scholar
  62. Zhu R, Bao T, Wang Q, Xu H, Liu Y (2014) Summertime CO2 fluxes and ecosystem respiration from marine animal colony tundra in maritime Antarctica. Atmos Environ 98:190–201CrossRefGoogle Scholar
  63. Zimov SA, Schuur EA, Chapin Iii FS (2006) Permafrost and the global carbon budget. Science 312:1612–1613CrossRefGoogle Scholar
  64. 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 Nature Switzerland AG 2019

Authors and Affiliations

  • Thamar Holanda da Silva
    • 1
  • Débora Amorim Saraiva Silva
    • 1
  • André Thomazini
    • 2
  • Carlos Ernesto Gonçalves Reynaud Schaefer
    • 3
  • Luiz Henrique Rosa
    • 1
  1. 1.Departamento de MicrobiologiaInstituto de Ciências Biológicas, Universidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Departamento de Ciências AgráriasUniversidade Federal de São João Del ReiSete LagoasBrazil
  3. 3.Departamento de SolosUniversidade Federal de ViçosaViçosaBrazil

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