Abstract
We evaluated the diversity and distribution of viable fungi present in permafrost and active layers obtained from three islands of Maritime Antarctica. A total of 213 fungal isolates were recovered from the permafrost, and 351 from the active layer, which were identified in 58 taxa; 27 from permafrost and 31 from the active layer. Oidiodendron, Penicillium, and Pseudogymnoascus taxa were the most abundant in permafrost. Bionectriaceae, Helotiales, Mortierellaceae, and Pseudeurotium were the most abundant in the active layer. Only five shared both substrates. The yeast Mrakia blollopis represented is the first reported on Antarctic permafrost. The fungal diversity detected was moderate to high, and composed of cosmopolitan, cold-adapted, and endemic taxa, reported as saprobic, mutualistic, and parasitic species. Our results demonstrate that permafrost shelters viable fungi across the Maritime Antarctica, and that they are contrasting to the overlying active layer. We detected important fungal taxa represented by potential new species, particularly, those genetically close to Pseudogymnoascus destructans, which can cause extinction of bats in North America and Eurasia. The detection of viable fungi trapped in permafrost deserves further studies on the extension of its fungal diversity and its capability to expand from permafrost to other habitats in Antarctica, and elsewhere.
Similar content being viewed by others
References
Adams BJ et al (2006) Diversity and distribution of Victoria land biota. Soil Biol Biochem 38:3003–3018. https://doi.org/10.1016/j.soilbio.2006.04.030
Adlam LS, Balks MR, Seybold CA, Campbell DI (2010) Temporal and spatial variation in active layer depth in the McMurdo sound region, Antarctica. Antarct Sci 22(1):45–52. https://doi.org/10.1017/S0954102009990460
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
Andersen NR, Rasmussen PR (1984) The constitution of clerocidin a new antibiotic isolated from Oidiodendron truncatum. Tetrahedron Lett 25:465–468. https://doi.org/10.1016/S0040-4039(00)99912-X
Arenz BE, Blanchette RA (2009) Investigations of fungal diversity in wooden structures and soils at historic sites on the Antarctic Peninsula. Can J Microbiol 55:46–56
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
Bakermans C, Tsapin AI, Souza-Egipsy V, Gilichinsky DA, Nealson KH (2003) Reproduction and metabolism at − 10 °C of bacteria isolated from Siberian permafrost. Environ Microbiol 5:321–326. https://doi.org/10.1046/j.1462-2920.2003.00419.x
Bardou P, Mariette J, Escudié F et al (2014) Jvenn: an interactive Venn diagram viewer. BMC Bioinform 15:293. https://doi.org/10.1186/1471-2105-15-293
Biskaborn BK et al (2019) Permafrost is warming at a global scale. Nat Commun 10:264. https://doi.org/10.1038/s41467-018-08240-4
Bockheim JG, Hall KJ (2002) Permafrost, active-layer dynamics and periglacial environments of continental Antarctica. S Afr J Sci 98:82–90
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
Buzzini P, Turk M, Perini L, Turchetti B, Gunde-Cimerman N (2017) Yeasts in polar and subpolar habitats. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: diversity. Springer, Berlin, pp 331–365 https://doi.org/10.1007/978-3-319-62683-3_11
Castella A (1967) Maintenance and cultivation of common pathogenic fungi of man in sterile distilled water. Further researches. J Trop Med Hyg 70:181
Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727. https://doi.org/10.1890/03-0557
Culmo RF, Swanson KJ, Brennan WP (1989) Application of the PE 2400 CHN and PE 2410 N for soils. Perkin-Elmer Publication EAN30, Norwalk
da Silva TH, Silva DAS, Thomazini A, Schaefer CEGR, Rosa LH (2019) antarctic permafrost: an unexplored fungal microhabitat at the edge of life. In: Rosa LH (ed) Fungi of Antarctica, 1st edn. Springer, Cham, pp 147–164 https://doi.org/10.1007/978-3-030-18367-7_7
De García V, Brizzio S, Libkind D, Buzzini P, Broock MV (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia Argentina. FEMS Microbiol Ecol 59:331–341. https://doi.org/10.1111/j.1574-6941.2006.00239.x
Del Frate G, Caretta G (1990) Fungi isolated from Antarctic material. Polar Biol 11:1–7. https://doi.org/10.1007/BF00236515
di Menna ME (1966) Yeasts in Antarctic soils. Antonie Van Leeuwenhoek 32:29–38. https://doi.org/10.1007/BF02097443
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 20:425–435. https://doi.org/10.1007/s00792-016-0833-y
Edgington S, Thompson E, Moore D, Hughes KA, Bridge P (2014) Investigating the insecticidal potential of Geomyces (Myxotrichaceae: Helotiales) and Mortierella (Mortierellacea: Mortierellales) isolated from Antarctica. Springer Plus 3:289. https://doi.org/10.1186/2193-1801-3-289
EMBRAPA, Empresa Brasileira de Pesquisa Agropecuária (1997) Centro Nacional de Pesquisa de Solos. Manual métodos de análise de solo, Rio de Janeiro, p 212
French HM (2007) The periglacial environment, 3rd edn. John Wiley and Sons, West Sussex, p 458
Furbino 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. https://doi.org/10.1007/s00248-014-0374-9
Gilichinsky DA et al (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology 7:275–311. https://doi.org/10.1089/ast.2006.0012
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 J 7:1434–1451. https://doi.org/10.1038/ismej.2013.77
Godinho VM, Gonçalves VN, Santiago IF, Figueredo HM, Vitoreli GA, Schaefer CE, Barbosa EC, Oliveira JG, Alves TM, Zani CL, Junior PA, Murta SM, 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
Godinho VM, de Paula MTR, Silva DAS, Paresque K, Martins AP, Colepicolo P, Rosa CA, Rosa LH (2019) Diversity and distribution of cryptic cultivable fungi associated with marine animals of Antarctica. Fungal Biol 123:507–516. https://doi.org/10.1016/j.funbio.2019.05.001
Gomes ECQ, Godinho VM, Silva DAS, De Paula MTR, Vitoreli GA, Zani CL et al (2018) Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites. Extremophiles 22:381–393. https://doi.org/10.1007/s00792-018-1003-1
Gonçalves VN, Vaz AB, 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, Carvalho CR, Johann S, Mendes G, Alves TMA, Zani CL, Junior PAS, Murta SMF, Romanha AJ, Cantrell CL, Rosa CA, Rosa LH (2015) Antibacterial, antifungal and antiprotozoal activities of fungal communities present in different substrates from Antarctica. Polar Biol 38:1143–1152. https://doi.org/10.1007/s00300-015-1672-5
Goordial J, Davila A, Lacelle D et al (2016) Nearing the cold-arid limits of microbial life in permafrost of an upper dry valley, Antarctica. ISME J 10:1613–1624. https://doi.org/10.1038/ismej.2015.239
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 Microb 19:443–458. https://doi.org/10.1111/1462-2920.13353
Guglielmin M, Cannone N (2012) A permafrost warming in a cooling Antarctica? Clim Change 111:177–195. https://doi.org/10.1007/s10584-011-0137-2
Hammer Ø, Harper DAT, Ryan PD (2001) PAST-palaeontological statistics, ver. 1.89. Palaeontol Electron 4:1–9
Hayes MA (2012) The Geomyces fungi: ecology and distribution. Bioscience 62:819–823. https://doi.org/10.1525/bio.2012.62.9.7
Henríquez M, Vergara K, Norambuena J, Beiza A, Maza F, Ubilla P, Araya I, Chávez R, SanMartín A, Darias J, Darias MJ, Vaca I (2014) Diversity of cultivable fungi associated with Antarctic marine sponges and screening for their antimicrobial, antitumoral and antioxidant potential. World J Microbiol Biotechnol 30:65–76. https://doi.org/10.1007/s11274-013-1418-x
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
Jansson JK, Taş N (2014) The microbial ecology of permafrost. Nat Rev Microbiol 12:414–425. https://doi.org/10.1038/nrmicro3262
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi. CAB International, Wallingford
Kochkina GA et al (2001) Survival of micromycetes and actinobacteria under conditions of long-term natural cryopreservation. Microbiology 70:356–364. https://doi.org/10.1023/A:1010419831245
Kochkina G, Ivanushkina N, Ozerskaya S, Chigineva N, Vasilenko O, Firsov S, Gilichinsky D (2012) Ancient fungi in Antarctic permafrost environments. FEMS Microbiol Ecol 82:501–509. https://doi.org/10.1111/j.1574-6941.2012.01442.x
Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73:331–371. https://doi.org/10.1023/A:1001761008817
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
Leushkin EV et al (2015) Comparative genome analysis of Pseudogymnoascus spp. reveals primarily clonal evolution with small genome fragments exchanged between lineages. BMC Genomics 16:400. https://doi.org/10.1186/s12864-015-1570-9
Li L, Li D, Luan Y, Gu Q, Zhu T (2012) Cytotoxic metabolites from the antarctic psychrophilic fungus Oidiodendron truncatum. J Nat Prod 75:920–927. https://doi.org/10.1021/np3000443
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 NA, Coleman JTH, Redell DN, Reeder DM, Blehert DS (2011) Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480:376–378
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
Madariaga-Mazón A, González-Andrade M, González MDC, Glenn AE, Cerda-García-Rojas CM, Mata R (2013) Absolute configuration of acremoxanthone C, a potent calmodulin inhibitor from Purpureocillium lilacinum. J Nat Prod 76:1454–1460. https://doi.org/10.1021/np4002477
Malkus A et al (2006) RNA polymerase II gene (RPB2) encoding the second largest protein subunit in Phaeosphaeria nodorum and P. avenaria. Mycol Res 110:1152–1164. https://doi.org/10.1016/j.mycres.2006.07.015
Melo IS, Santos SN, Rosa LH, Parma MM, Silva LJ, Queiroz SC, Pellizari VH (2014) Isolation and biological activities of an endophytic Mortierella alpina strain from the Antarctic moss Schistidium antarctici. Extremophiles 18:15–23. 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
Morrison VA (2006) Echinocandin antifungals: review and update. Expert Rev Anti-Infect Ther 4:325–342. https://doi.org/10.1586/14787210.4.2.325
Newsham KK, Garnett MH, Robinson CH, Cox F (2018) Discrete taxa of saprotrophic fungi respire different ages of carbon from Antarctic soils. Sci Rep 8:7866. https://doi.org/10.1038/s41598-018-25877-9
Nikrad MP, Kerkhof LJ, Häggblom MM (2016) The subzero microbiome: microbial activity in frozen and thawing soils. FEMS Microbiol Ecol 92:fiw081. https://doi.org/10.1093/femsec/fiw081
O'Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233
Onofri S, Selbmann L, Zucconi L, Pagano S (2004) Antarctic microfungi as models for exobiology. Planet Space Sci 52:229–237. https://doi.org/10.1016/j.pss.2003.08.019
Ozerskaya S, Kochkina G, Ivanushkina N, Gilichinsky DA (2009) Fungi in permafrost. In: Margesin R (ed) Permafrost soils. Springer, Berlin, pp 85–95 https://doi.org/10.1007/978-3-540-69371-0_7
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. Curr Microbiol 60:307–314. https://doi.org/10.1007/s00284-009-9543-3
Peláez F et al (2011) Phylogeny and intercontinental distribution of the pneumocandin-producing anamorphic fungus Glarea lozoyensis. Mycology 2:1–17. https://doi.org/10.1080/21501203.2010.544334
Perdomo H, Cano J, Gené J, García D, Hernández M, Guarro J (2013) Polyphasic analysis of Purpureocillium lilacinum isolates from different origins and proposal of the new species Purpureocillium lavendulum. Mycologia 105:151–161. https://doi.org/10.3852/11-190
Ping CL, Bockheim JG, Kimble JM, Michaelson GJ, Walker DA (1998) Characteristics of cryogenic soils along a latitudinal transect in arctic Alaska. J Geophys Res 103:2891–2892. https://doi.org/10.1029/98JD02024
Potapowicz J, Szumińska D, Szopińska M, Polkowska Ż (2019) The influence of global climate change on the environmental fate of anthropogenic pollution released from the permafrost. Part I. Case study of Antarctica. Sci Total Environ 651:1534–1548. https://doi.org/10.1016/j.scitotenv.2018.09.168
Rice AV, Currah RS (2006) Two new species of Pseudogymnoascus with Geomyces anamorphs and their phylogenetic relationship with Gymnostellatospora. Mycologia 98:307–318. https://doi.org/10.1080/15572536.2006.11832703
Rosa LH, Vaz AB, 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 et al (2019) Fungi in Antarctica: diversity, ecology, effects of climate change, and bioprospection for bioactive compounds. In: Rosa LH (ed) Fungi of Antarctica. Springer, Cham, pp 1–17 https://doi.org/10.1007/978-3-030-18367-7_1
Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Bio 6:127–141. https://doi.org/10.1007/s11157-006-9107-y
Schaefer CEGR, Pereira TTC, Almeida ICC, Michel RFM, Correa GR, Figueiredo LPS, Ker JC (2016) Penguin activity modify the thermal regime of active layer in Antarctica: a case study from Hope Bay. CATENA 149:582–591. https://doi.org/10.1016/j.catena.2016.07.021
Semenova TA, Morgado LN, Welker JM, Walker MD, Smets E, Geml J (2015) Long-term experimental warming alters community composition of ascomycetes in Alaskan moist and dry Arctic tundra. Mol Ecol 24:424–437. https://doi.org/10.1111/mec.13045
Shuey MM, Drees KP, Lindner DL, Keim P, Foster JT (2014) Highly sensitive quantitative PCR for the detection and differentiation of Pseudogymnoascus destructans and other Pseudogymnoascus species. Appl Environ Microbiol 80:1726–1731. https://doi.org/10.1128/AEM.02897-13
Simas FN, Schaefer CE, Michel RF, Francelino MR, Bockheim JG (2015) Soils of the South Orkney and South Shetland Islands, Antarctica. In: Bockheim JG (ed) The soils of Antarctica. Springer, Cham, Switzerland, pp 227–273 https://doi.org/10.1007/978-3-319-05497-1_13
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
Steven B, Leveille R, Pollard WH, Whyte LG (2006) Microbial ecology and biodiversity in permafrost. Extremophiles 10:259–267. https://doi.org/10.1007/s00792-006-0506-3
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, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov SA (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Glob Biogeochem 23:GB2023. https://doi.org/10.1029/2008GB003327
Thomas-Hall SR, Turchetti B, Buzzini P, Branda E, Boekhout T, Theelen B, Watson K (2010) Cold-adapted yeasts from Antarctica and the Italian Alps—description of three novel species: Mrakia robertii sp. nov., Mrakia blollopis sp. nov. and Mrakiella niccombsii sp. nov. Extremophiles 14:47–59. https://doi.org/10.1007/s00792-009-0286-7
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
Tsuji M, Yokota Y, Shimohara K, Kudoh S, Hoshino T (2013) An application of wastewater treatment in a cold environment and stable lipase production of Antarctic basidiomycetous yeast Mrakia blollopis. PLoS ONE. https://doi.org/10.1371/journal.pone.0059376
Vaca I, Chávez R (2019) Bioactive compounds produced by Antarctic filamentous fungi. In: Rosa L (ed) Fungi of Antarctica. Springer, Cham, pp 265–283 https://doi.org/10.1007/978-3-030-18367-7_12
Vieira G et al (2010) Thermal state of permafrost and active-layer monitoring in the Antarctic: advances during the international polar year 2007–2009. Permafr Periglac 21:182–197. https://doi.org/10.1002/ppp.685
Vorobyova E, Minkovsky N, Mamukelashvili A, Zvyagintsev D, Soina V, Polanskaya L, Gilichinsky D (2001) Micro-organisms and biomarkers in permafrost. In: Paepe R, Melnikov VP, Van Overloop E, Gorokhov VD (eds) Permafrost response on economic development, environmental security and natural resources. Springer, Dordrecht, pp 527–541 https://doi.org/10.1007/978-94-010-0684-2_36
Wentzel LCP, Inforsato FJ, Montoya QV, Rossin BG, Nascimento NR, Rodrigues A, Sette LD (2019) Fungi from admiralty bay (King George Island, Antarctica) soils and marine sediments. Microb Ecol 77:12–24. https://doi.org/10.1007/s00248-018-1217-x
White TJ, Bruns T, Lee SJWT, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322
WRB World Reference Base for Soil Resources (2014) International soil classification system for naming soils and creating legends for soil maps. FAO, Rome
Xin MX, Zhou PJ (2007) Mrakia psychrophila sp. nov., a new species isolated from Antarctic soil. J Zhejiang Univ Sci B 8:260–265. https://doi.org/10.1631/jzus.2007.B0260
Yurkov AM, Sannino C, Turchetti B (2019) Mrakia fibulata sp. Nov., a psychrotolerant yeast from temperate and cold habitats. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-019-01359-4
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
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. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
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
da Silva, T.H., Silva, D.A.S., de Oliveira, F.S. et al. Diversity, distribution, and ecology of viable fungi in permafrost and active layer of Maritime Antarctica. Extremophiles 24, 565–576 (2020). https://doi.org/10.1007/s00792-020-01176-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-020-01176-y