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.
Similar content being viewed by others
References
Abyzov SS (1993) Microorganisms in the Antarctic ice. In: Friedmann EI (ed) Antarctic microbiology. Wiley, New York, pp 265–295
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
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
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
Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27:219–225
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
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
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
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
Buzzini P, Turchetti B, Yurkov A (2018) Extremophilic yeasts: the toughest yeasts around? Yeast 35:487–497
Callahan HL, Portal AC, Devereaux R, Grogl M (1997) An axenic amastigote system for drug screening. Antimicrob Agents Chemother 41:818–822
Castellani A (1967) Maintenance and cultivation of common pathogenic fungi in distilled water. J Trop Med Hyg 42:181–184
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
Dayan FE, Romagni JG, Duke SO (2000) Investigating the mode of action of natural phytotoxins. J Chem Ecol 26:2079–2094
D’Elia T, Veerapaneni R, Theraisnathan V, Rogers SO (2009) Isolation of fungi from Lake Vostok accretion ice. Mycologia 101:751–763
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
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
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
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
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
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
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
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
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
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
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
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
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Paleontol Electron 4:1–9
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
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
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi. CAB International, Wallingford
Knowlton C, Veerapaneni R, D’Elia RSO (2013) Microbial analyses of ancient ice core sections from Greenland and Antarctica. Biology 2:206–232
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
Kornerup A, Wanscher JH (1984) Methuen handbook of colour. Eyre Methuen, London
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
Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study. Elsevier, Amsterdam
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
Lutz S, Anesio AM, Edwards A, Benning LG (2015) Microbial diversity on Icelandic glaciers and ice caps. Front Microbiol 6:307
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
Margesin R, Collins T (2019) Microbial ecology of the cryosphere (glacial and permafrost habitats): current knowledge. Appl Microbiol Biotechnol 103:2537–2549
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
Montemartini A, Caretta G, Del Frate G (1993) Notes on Thelebolus microsporus isolated in Antarctica. Mycotaxon 48:343–358
Nicoletti R, Trincone A (2016) Bioactive compounds produced by strains of Penicillium and Talaromyces of marine origin. Mar Drugs 14:1–35
Perini L, Gostinčar C, Gunde-Cimerman N (2019a) Fungal and bacterial diversity of Svalbard subglacial ice. Sci Rep 9:1–15
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
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
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
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
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
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
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
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
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
Sonjak S, Frisvad JC, Gunde-Cimerman N (2006) Penicillium mycobiota in Arctic subglacial ice. Microb Ecol 50:207–216
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
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
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
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
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Oren.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-020-01161-5