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Fungi in glacial ice of Antarctica: diversity, distribution and bioprospecting of bioactive compounds

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Abstract

We identified cultivable fungi present in the glacial ice fragments collected in nine sites across Antarctica Peninsula and assessed their abilities to produce bioactive compounds. Three ice fragments with approximately 20 kg were collected, melted and 3 L filtered through of 0.45 µm sterilized membranes, which were placed on the media Sabouraud agar and minimal medium incubated at 10 °C. We collected 66 isolates classified into 27 taxa of 14 genera. Penicillium palitans, Penicillium sp. 1, Thelebolus balaustiformis, Glaciozyma antarctica, Penicillium sp. 7, Rhodotorula mucilaginosa, and Rhodotorula dairenensis had the highest frequencies. The diversity and richness of the fungal community were high with moderate dominance. Penicillium species were present in all samples, with Penicillium chrysogenum showing the broadest distribution. P. chrysogenum, P. palitans, and Penicillium spp. had trypanocidal, leishmanicidal, and herbicidal activities, with P. chrysogenum having the broadest and highest capability. 1H NMR signals revealed the presence of highly functionalized secondary metabolites in the bioactive extracts. Despite extreme environmental conditions, glacial ice harbours a diverse fungal community, including species never before recorded in the Arctic and Antarctica. Among them, Penicillium taxa may represent wild fungal strains with genetic and biochemical pathways that may produce new secondary bioactive metabolites.

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References

  • Abyzov SS (1993) Microorganisms in the Antarctic ice. In: Friedmann EI (ed) Antarctic microbiology. Wiley, New York, pp 265–295

    Google Scholar 

  • Abyzov SS, Hoover RB, Imura S, Mitskevich IN, Naganuma T, Poglazova MN, Ivanov MV (2004) Use of different methods for discovery of ice-entrapped microorganisms in ancient layers of the Antarctic glacier. Adv Space Res 33:1222–1230

    Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Alves IM, Gonçalves VN, Oliveira FS, Schaefer CE, Rosa CA, Rosa LH (2019) The diversity, distribution, and pathogenic potential of cultivable fungi present in rocks from the South Shetlands archipelago, Maritime Antarctica. Extremophiles 23:327–336

    PubMed  Google Scholar 

  • Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27:219–225

    PubMed  Google Scholar 

  • Antipova TV, Zhelifonova VP, Baskunov BP, Kochkina GA, Ozerskaya SM, Kozlovskii AG (2018) Exometabolites the penicillium fungi isolated from various high-latitude ecosystems. Microbiology 87:642–651

    CAS  Google Scholar 

  • Bovio E, Garzoli L, Poli A, Prigione V, Firsova D, McCormack GP, Varese GC (2018) The culturable mycobiota associated with three Atlantic sponges, including two new species: Thelebolus balaustiformis and T. spongiae. Fungal Syst Evol 1:141–167

    PubMed  PubMed Central  Google Scholar 

  • Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369

    PubMed  CAS  Google Scholar 

  • Brunati M, Rojas JL, Sponga F et al (2009) Diversity and pharmaceutical screening of fungi from benthic mats of Antarctic lakes. Mar Genom 2:43–50

    Google Scholar 

  • Buzzini P, Turchetti B, Yurkov A (2018) Extremophilic yeasts: the toughest yeasts around? Yeast 35:487–497

    PubMed  CAS  Google Scholar 

  • Callahan HL, Portal AC, Devereaux R, Grogl M (1997) An axenic amastigote system for drug screening. Antimicrob Agents Chemother 41:818–822

    PubMed  PubMed Central  CAS  Google Scholar 

  • Castellani A (1967) Maintenance and cultivation of common pathogenic fungi in distilled water. J Trop Med Hyg 42:181–184

    Google Scholar 

  • Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G (2004) MycoBank: an online initiative to launch mycology into the 21st century. Stud Mycol 50:19–22

    Google Scholar 

  • Dayan FE, Romagni JG, Duke SO (2000) Investigating the mode of action of natural phytotoxins. J Chem Ecol 26:2079–2094

    CAS  Google Scholar 

  • D’Elia T, Veerapaneni R, Theraisnathan V, Rogers SO (2009) Isolation of fungi from Lake Vostok accretion ice. Mycologia 101:751–763

    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 

  • de Menezes GCA, Porto BA, Simões JC, Rosa CA, Rosa LH (2019) Fungi in snow and glacial ice of Antarctica. In: Rosa LH (ed) Fungi of Antarctica, 1st edn. Springer, Basel, pp 127–146

    Google Scholar 

  • Duo Saito RA, Connell L, Rodriguez R, Redman R, Libkind D, de Garcia V (2018) Metabarcoding analysis of the fungal biodiversity associated with Castaño Overa Glacier—Mount Tronador, Patagonia, Argentina. Fungal Ecol 36:8–16

    Google Scholar 

  • Fell JW, Statzell AC, Hunter IL, Phaff L (1969) Leucosporidium gen. n., the heterobasidiomycetous stage of several yeasts of the genus Candida. Antonie Van Laeuwenhoek 35:433–462

    CAS  Google Scholar 

  • 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 peninsula. Microb Ecol 67:775–787

    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  PubMed Central  CAS  Google Scholar 

  • 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 7:1434–1451

    PubMed  PubMed Central  CAS  Google Scholar 

  • Godinho VM, Gonçalves VN, Santiago IF et al (2015) Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 19:585–596

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Gonçalves DB, Teixeira JA, Bazzolli DMS, de Queiroz MV, de Araújo EF (2012b) Use of response surface methodology to optimize production of pectinases by recombinant Penicillium griseoroseum T20. Biocatal Agric Biotechnol 1:140–146

    Google Scholar 

  • Gonçalves VN, Oliveira FS, Carvalho CR, Schaefer CEGR, Rosa CA, Rosa LH (2017) Antarctic rocks from continental Antarctica as source of potential human opportunistic fungi. Extremophiles 21:851–860

    PubMed  Google Scholar 

  • Gunde-Cimerman N, Sonjak S, Zalar P, Frisvad JC, Diderichsen B, Plemenitaš A (2003) Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity. Phys Chem Earth Parts A/B/C 28:1273–1278

    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 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Index Fungorum Partnership (2016) Index Fungorum. Checklist dataset. http://www.indexfungorum.org. Accessed 24 May 2019

  • Jacobs PH, Taylor HC, Shafer JC (1964) Studies of fungi at Amundsen-Scott IGY South Pole Base (1957). Arch Dermatol 89:117–123

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Knowlton C, Veerapaneni R, D’Elia RSO (2013) Microbial analyses of ancient ice core sections from Greenland and Antarctica. Biology 2:206–232

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kobayasi Y, Hiratsuka N, Korf RP, Tubaki K, Aoshima K, Soneda M, Sugiyama J (1967) Mycological studies of the Alaskan Arctic. Annu Rep Inst Ferment Osaka 3:1–138

    Google Scholar 

  • Kornerup A, Wanscher JH (1984) Methuen handbook of colour. Eyre Methuen, London

    Google Scholar 

  • Kozlovsky AG, Kochkina GA, Zhelifonova VP, Antipova TV, Ivanushkina NE, Ozerskaya SM (2020) Secondary metabolites of the genus Penicillium from undisturbed and anthropogenically altered Antarctic habitats. Folia Microbiol 65:95–102

    CAS  Google Scholar 

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

    Google Scholar 

  • 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 45:172–177

    PubMed  CAS  Google Scholar 

  • Lutz S, Anesio AM, Edwards A, Benning LG (2015) Microbial diversity on Icelandic glaciers and ice caps. Front Microbiol 6:307

    PubMed  PubMed Central  Google Scholar 

  • Malkus A, Chang PFL, Zuzga SM, Chung KR, Shao J, Cunfer BM, Arseniuk E, Ueng PP (2006) RNA polymerase II gene (RPB2) encoding the second largest protein subunit in Phaeosphaeria nodorum and P. avenaria. Mycological Res 110:1152–1164

    CAS  Google Scholar 

  • Margesin R, Collins T (2019) Microbial ecology of the cryosphere (glacial and permafrost habitats): current knowledge. Appl Microbiol Biotechnol 103:2537–2549

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nicoletti R, Trincone A (2016) Bioactive compounds produced by strains of Penicillium and Talaromyces of marine origin. Mar Drugs 14:1–35

    Google Scholar 

  • Perini L, Gostinčar C, Gunde-Cimerman N (2019a) Fungal and bacterial diversity of Svalbard subglacial ice. Sci Rep 9:1–15

    CAS  Google Scholar 

  • Perini L, Gostinčar C, Anesio AM, Williamson C, Tranter M, Gunde-Cimerman N (2019b) Darkening of the Greenland ice sheet: fungal abundance and diversity are associated with algal bloom. Front Microbiol 10:1–14

    Google Scholar 

  • Rogers SO, Theraisnathan V, Ma LJ, Zhao Y, Zhang G, Shin SG, Castello JD, Starmer WT (2004) Comparisons of protocols for decontamination of environmental ice samples for biological and molecular examinations. Appl Environ Microbiol 70:2540–2544

    PubMed  PubMed Central  CAS  Google Scholar 

  • Romanha AJ, de Castro SL, Soeiro MNC et al (2010) In vitro and in vivo experimental models for drug screening and development for Chagas disease. Mem Inst Oswaldo Cruz 105:233–238

    PubMed  CAS  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

    Google Scholar 

  • Rosa LH, Queiroz SCN, Moraes RM, Wang X, Techen N, Pan Z, Cantrell C, 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

    Google Scholar 

  • Rosa LH, Zani CL, Cantrell CL, Duke SO, Dijck PV, 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, 1st edn. Springer, Cham, pp 1–17

    Google Scholar 

  • Sampaio JP (2004) Diversity, phylogeny and classification of basidiomycetous yeasts. In: Agerer R, Blanz P, Piepenbring M (eds) Frontiers in Basidiomycete mycology, 1st edn. IHW-Verlag, Verlagsbuchhandlung, pp 49–80

    Google Scholar 

  • Sanyal A, Antony R, Samui G, Thamban M (2018) Microbial communities and their potential for degradation of dissolved organic carbon in cryoconite role environments of Himalaya and Antarctica. Microbiol Res 208:32–42

    PubMed  CAS  Google Scholar 

  • Sazanova KV, Senik SV, Kirtsideli IY, Shavarda AL (2019) Metabolomic profiling and lipid composition of Arctic and Antarctic strains of Micromycetes Geomyces pannorum and Thelebolus microsporus grown at different temperatures. Microbiology 88:282–291

    CAS  Google Scholar 

  • Sonjak S, Frisvad JC, Gunde-Cimerman N (2006) Penicillium mycobiota in Arctic subglacial ice. Microb Ecol 50:207–216

    Google Scholar 

  • Sonjak S, Frisvad JC, Gunde-Cimerman N (2007a) Genetic variation among Penicillium crustosum isolates from arctic and other ecological niches. Microb Ecol 54:298–305

    PubMed  CAS  Google Scholar 

  • Sonjak S, Uršič V, Frisvad JC, Gunde-Cimerman N (2007b) Penicillium svalbardense, a new species from Arctic glacial ice. Antonie Van Leeuwenhoek 92:43–51

    PubMed  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    PubMed  PubMed Central  CAS  Google Scholar 

  • Turchetti B, Hall SRT, Connell LB, Branda E, Buzzini P, Theelen B, Müller WH, Boekhout T (2011) Psychrophilic yeasts from Antarctica and European glaciers: description of Glaciozyma gen. nov., Glaciozyma martinii sp. nov. and Glaciozyma watsonii sp. nov. Extremophiles 15:573–586

    PubMed  CAS  Google Scholar 

  • Vanderwolf KJ, Malloch D, McAlpine DF (2018) Psychrotolerant microfungi associated with deer mice (Peromyscus maniculatus) in a White-nose Syndrome positive bat hibernaculum in eastern Canada. Can Field Nat 131:238–245

    Google Scholar 

  • Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N, Gupta VK, Saxena AK (2018) Biodiversity of the genus Penicillium in different habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 3–18

    Google Scholar 

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Acknowledgements

We acknowledge the financial support from PROANTAR CNPq (442258/2018-6), INCT Criosfera, FAPEMIG, CAPES, FNDCT, MCTIC and PRPq-UFMG. GCA de Menezes scholarship was supported by CNPq (142341/2018-5) and FAPEMIG (418).

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Correspondence to Luiz Henrique Rosa.

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de Menezes, G.C.A., Porto, B.A., Amorim, S.S. et al. Fungi in glacial ice of Antarctica: diversity, distribution and bioprospecting of bioactive compounds. Extremophiles 24, 367–376 (2020). https://doi.org/10.1007/s00792-020-01161-5

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