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.
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References
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 25:3389–3402
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
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
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
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
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
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
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
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
Callahan HL, Portal AC, Devereaux R, Grogl M (1997) An axenic amastigote system for drug screening. Antimicrob Agents Chemother 41:818–822
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
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
Defelipo BV, Ribeiro AC (1981) Análise química de solos (metodologia). Viçosa, Brasil
di Menna ME (1966) Yeasts in Antarctic soils. Antonie Van Leeuwenhoek 32:29–38. https://doi.org/10.1007/BF02097443
EMBRAPA (1997) Manual de métodos de análise de solo. EMBRAPA-CNPS, Brasil
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
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
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
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
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, 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
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
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
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
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
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Hou CT (2008) New bioactive fatty acids. Asia Pac J Clin Nutr 17(S1):192–195
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
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi. CAB International, Wallingford
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
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
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
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
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
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
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
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
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
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
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 18:15–23
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
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
Mossman T (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55–63
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
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
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
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
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
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
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
Rudolph ED (1970) Local dissemination of plant propagules in Antarctica. In: Holdgate MW (ed) Antarctic Ecology, vol 2. Academic Press, London
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
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 1873–1927
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
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
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
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 47–59
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
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
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
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
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 28:15–22
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
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
Tatur A (1989) Ornithogenic soils of the maritime antarctic. Polish Pol Res 4:481–532
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
Tatur A, Myrcha A (1984) Ornithogenic soils on King George Island (maritime Antarctic zone). Polish Pol Res 5:31–60
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
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
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
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
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
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
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 315–322
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
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
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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.
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Gomes, E.C.Q., Godinho, V.M., Silva, D.A.S. et al. Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites. Extremophiles 22, 381–393 (2018). https://doi.org/10.1007/s00792-018-1003-1
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DOI: https://doi.org/10.1007/s00792-018-1003-1