Abstract
Yeasts have been frequently isolated from cold habitats, but their contribution to essential ecological processes such as the mineralization of organic matter in these environments is less known. Here, the diversity, metabolic capability, and extracellular enzyme profiles of yeasts from snow, blue ice and cryoconite hole environments from East Antarctica and cryoconite holes from a glacier in Western Himalaya were determined. Eighty-six yeast strains isolated were affiliated to the genera Glaciozyma, Goffeauzyma, Mrakia, Phenoliferia, and Rhodotorula. Variations in the abundance, diversity, physiological properties, extracellular enzyme and carbon substrate utilization patterns of the isolated yeasts, reflect the specific environmental conditions from which they were isolated. Overall, 20–90% of the yeasts across all habitat types and geographical locations produced extracellular enzymes to degrade proteins, esters, carbohydrates, pectin, cellulose, lignin, and tannin. About 10 and 29% of the yeasts also exhibited ability to solubilize rock-minerals like phosphate and silicate, respectively. Additionally, selected isolates were able to metabolize 28–93% of the carbon substrates comprising different compound classes on Biolog YT plates. Overall, the ability of yeasts to use diverse organic compounds prevalent on the glacier surface, points to their ecological significance in the decomposition of organic matter, cycling of nutrients, and in the weathering of minerals in supraglacial environments. Moreover, their wide metabolic capabilities suggest that they can colonize new niches and environments when meltwater export during the summer that enables links with surrounding ecosystems.
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The ITS region and D1/D2 domain of the 26S rRNA gene sequence data generated from this study have been submitted to the NCBI database.
References
An Y, Xu J, Feng L, Zhang X, Liu Y, Kang S et al (2019) Molecular characterization of organic aerosol in the Himalayas: insight from ultra-high-resolution mass spectrometry. Atmos Chem Phys 19(2):1115–1128
Anesio AM, Hodson AJ, Fritz A, Psenner R, Sattler B (2009) High microbial activity on glaciers: importance to the global carbon cycle. Glob Change Biol 15(4):955–960
Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27(4):219–225
Anesio AM, Sattler B, Foreman C, Telling J, Hodson A, Tranter M, Psenner R (2010) Carbon fluxes through bacterial communities on glacier surfaces. Ann Glaciol 51(56):32–40
Antony R, Grannas AM, Willoughby AS, Sleighter RL, Thamban M, Hatcher PG (2014) Origin and sources of dissolved organic matter in snow on the East Antarctic ice sheet. Environ Sci Technol 48(11):6151–6159
Antony R, Mahalinganathan K, Thamban M, Nair S (2011) Organic carbon in Antarctic snow: spatial trends and possible sources. Environ Sci Technol 45(23):9944–9950
Antony R, Sanyal A, Kapse N, Dhakephalkar PK, Thamban M, Nair S (2016) Microbial communities associated with Antarctic snow pack and their biogeochemical implications. Microbiol Res 192:192–202
Antony R, Willoughby AS, Grannas AM, Catanzano V, Sleighter RL, Thamban M et al (2017) Molecular insights on dissolved organic matter transformation by supraglacial microbial communities. Environ Sci Technol 51(8):4328–4337
Antony R, Krishnan KP, Laluraj CM, Thamban M, Dhakephalkar PK, Engineer AS, Shivaji S (2012) Diversity and physiology of culturable bacteria associated with a coastal Antarctic ice core. Microbiol Res 167(6):372–380
Banfield JF, Barker WW, Welch SA, Taunton A (1999) Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proc Natl Acad Sci 96(7):3404–3411
Barker WW, Banfield JF (1996) Biologically versus inorganically mediated weathering reactions: relationships between minerals and extracellular microbial polymers in lithobiontic communities. Chem Geol 132(1–4):55–69
Barker WW, Banfield JF (1998) Zones of chemical and physical interaction at interfaces between microbial communities and minerals: a model. Geomicrobiol J 15(3):223–244
Bradley JA, Singarayer JS, Anesio AM (2014) Microbial community dynamics in the forefield of glaciers. Proc R Soc B 281(1795):20140882
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(3):354–369
Breitenbach R, Silbernagl D, Toepel J, Sturm H, Broughton WJ, Sassaki GL, Gorbushina AA (2018) Corrosive extracellular polysaccharides of the rock-inhabiting model fungus Knufia petricola. Extremophiles 22(2):165–175
Butinar L, Spencer-Martins I, Gunde-Cimerman N (2007) Yeasts in high Arctic glaciers: the discovery of a new habitat for eukaryotic microorganisms. Antonie Leeuwenhoek 91(3):277–289
Buzzini P, Lachance MA, Yurkov A (eds) (2017) Yeasts in natural ecosystems: diversity. Springer, Berlin
Buzzini P, Turchetti B, Diolaiuti G, D’Agata C, Martini A (2005) Culturable yeasts in meltwaters draining from two glaciers in the Italian Alps. Ann Glaciol 40:119–122
Carrasco M, Rozas JM, Barahona S, Alcaíno J, Cifuentes V, Baeza M (2012) Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiol 12(1):251
Choudhary P, Routh J, Chakrapani GJ (2010) Organic geochemical record of increased productivity in Lake Naukuchiyatal, Kumaun Himalayas, India. Environ Earth Sci 60(4):837–843
Chowdhury SP, Khanna S, Verma SC, Tripathi AK (2004) Molecular diversity of tannic acid degrading bacteria isolated from tannery soil. J Appl Microbiol 97(6):1210–1219
Collins T, Margesin R (2019) Psychrophilic lifestyles: mechanisms of adaptation and biotechnological tools. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-019-09659-5
Connell L, Redman R, Craig S, Scorzetti G, Iszard M, Rodriguez R (2008) Diversity of soil yeasts isolated from South Victoria Land. Antarctica Microbiol Ecol 56(3):448–459
Cook J, Edwards A, Takeuchi N, Irvine-Fynn T (2016) Cryoconite: the dark biological secret of the cryosphere. Prog Phys Geogr 40(1):66–111
Costa OY, Raaijmakers JM, Kuramae EE (2018) Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Front Microbiol 9:1636
De García V, Brizzio S, Libkind D, Buzzini P, Van Broock M (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia. Argentina FEMS Microbiol Ecol 59(2):331–341
de Garcia V, Brizzio S, van Broock MR (2012) Yeasts from glacial ice of Patagonian Andes, Argentina. FEMS Microbiol Ecol 82(2):540–550
de Garcia V, Trochine A, Uetake J, Bellora N, Libkind D (2020) Novel yeast taxa from the cold: description of Cryolevonia giraudoae sp. nov. and Camptobasidium gelus sp. nov. Int J Syst Evol Microbiol, ijsem004223
Duarte AWF, Dayo-Owoyemi I, Nobre FS, Pagnocca FC, Chaud LCS, Pessoa A, Sette LD (2013) Taxonomic assessment and enzymes production by yeasts isolated from marine and terrestrial Antarctic samples. Extremophiles 17(6):1023–1035
Edwards A, Douglas B, Anesio AM, Rassner SM, Irvine-Fynn TD, Sattler B, Griffith GW (2013) A distinctive fungal community inhabiting cryoconite holes on glaciers in Svalbard. Fungal Ecol 6(2):168–176
Feng L, Xu J, Kang S, Li X, Li Y, Jiang B, Shi Q (2016) Chemical composition of microbe-derived dissolved organic matter in cryoconite in Tibetan Plateau glaciers: insights from Fourier transform ion cyclotron resonance mass spectrometry analysis. Environ Sci Technol 50(24):13215–13223
Foster JL, Fogleman JC (1993) Identification and ecology of bacterial communities associated with necroses of three cactus species. Appl Environ Microbiol 59:1–6
Garcia-Lopez E, Cid C (2017) Glaciers and ice sheets as analog environments of potentially habitable icy worlds. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01407
Hatha AA, Rahiman MK, Krishnan KP, Saramma AV, Saritha G, Deepu L (2013) Characterisation and bioprospecting of cold adapted yeast from water samples of Kongsfjord, Norwegian Arctic
Hawkings J, Wadham J, Tranter M, Telling J, Bagshaw E, Beaton A et al (2016) The Greenland Ice Sheet as a hot spot of phosphorus weathering and export in the Arctic. Glob Biogeochem Cycles 30:191–210. https://doi.org/10.1002/2015GB005237
Hawkings JR, Wadham JL, Benning LG, Hendry KR, Tranter M, Tedstone A, Nienow P, Raiswell R (2017) Ice sheets as a missing source of silica to the polar oceans. Nat Commun 8:14198
Hock R, de Woul M, Radić V, Dyurgerov M (2009) Mountain glaciers and ice caps around Antarctica make a large sea‐level rise contribution. Geophys Res Lett 36(7)
Hood E, Battin TJ, Fellman J, O’neelSpencer SRG (2015) Storage and release of organic carbon from glaciers and ice sheets. Nat Geosci 8(2):91–96
Kang SM, Waqas M, Shahzad R, You YH, Asaf S, Khan MA et al (2017) Isolation and characterization of a novel silicate-solubilizing bacterial strain Burkholderia eburnea CS4–2 that promotes growth of japonica rice (Oryza sativa L. cv, Dongjin). Soil Sci Plant Nutr 63(3):233–241
Kaštovská K, Stibal M, Šabacká M, Černá B, Šantrůčková H, Elster J (2007) Microbial community structure and ecology of subglacial sediments in two polythermal Svalbard glaciers characterized by epifluorescence microscopy and PLFA. Polar Biol 30(3):277–287
Lachance MA, Starmer WT (1982) Evolutionary significance of physiological relationships among yeast communities associated with trees. Can J Bot 60:285–293
Libkind D, Brizzio S, Ruffini A, Gadanho M, van Broock M, Sampaio JP (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Antonie Leeuwenhoek 84(4):313–322
Lutz S, Anesio AM, Edwards A, Benning LG (2015) Microbial diversity on Icelandic glaciers and ice caps. Front Microbiol 6:307
Maharana AK (2016) Extracellular cold active endoglucanase and pigment producing psychrotolerant Penicillium pinophilum
Margesin R (2014) Bioremediation and biodegradation of hydrocarbons by cold-adapted yeasts in cold-adapted yeasts. Springer, Berlin, pp 465–480
Margesin R (ed) (2017) Psychrophiles: from biodiversity to biotechnology, vol 2. Springer, Berlin
Margesin R, Zacke G, Schinner F (2002) Characterization of heterotrophic microorganisms in alpine glacier cryoconite. Arct Antarct Alp Res 34(1):88–93
Merín MG, Martín MC, Rantsiou K, Cocolin L, de Ambrosini VIM (2015) Characterization of pectinase activity for enology from yeasts occurring. Argentine Bonarda Grape Braz J Microbiol 46(3):815–823
Musilova M, Tranter M, Bamber JL, Takeuchi N, Anesio AM (2016) Experimental evidence that microbial activity lowers the albedo of glaciers. Geochem Perspect Lett 2:106–116
Nakagawa T, Nagaoka T, Taniguchi S, Miyaji T, Tomizuka N (2004) Isolation and characterization of psychrophilic yeasts producing cold-adapted pectinolytic enzymes. Lett Appl Microbiol 38(5):383–387
Nazir R, Zaffar MR, Amin I (2019) Bacterial biofilms: the remarkable heterogeneous biological communities and nitrogen fixing microorganisms in lakes. Academic Press, Freshwater Microbiology, pp 307–340
Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species
Rampelotto PH (2010) Resistance of microorganisms to extreme environmental conditions and its contribution to astrobiology. Sustainability 2:1602–1623. https://doi.org/10.3390/su2061602
Rühland K, Phadtare NR, Pant RK, Sangode SJ, Smol JP (2006) Accelerated melting of Himalayan snow and ice triggers pronounced changes in a valley peatland from northern India. Geophys Res Lett 33(15)
Samui G, Antony R, Mahalinganathan K, Thamban M (2017) Spatial variability and possible sources of acetate and formate in the surface snow of East Antarctica. J Environ Sci 57:258–269
Samui G, Antony R, Thamban M (2018) Chemical characteristics of hydrologically distinct cryoconite holes in coastal Antarctica. Ann Glaciol 59(77):69–76
Samui GD (2019) Biogeochemistry of selected supraglacial ecosystems in coastal Antarctica. Doctoral dissertation, Goa University
Samui G, Antony R, Thamban M (2020) Fate of dissolved organic carbon in Antarctic Surface Environments during Summer. J Geophys Res-Biogeo, forthcoming
Sanyal A, Antony R, Samui G, Thamban M (2018) Microbial communities and their potential for degradation of dissolved organic carbon in cryoconite hole environments of Himalaya and Antarctica. Microbiol Res 208:32–42
Selbmann L, Zucconi L, Isola D, Onofri S (2015) Rock black fungi: excellence in the extremes, from the Antarctic to space. Curr Genet 61(3):335–345
Shivaji S, Bhadra B, Rao RS, Pradhan S (2008) Rhodotorula himalayensis sp. Nov., a novel psychrophilic yeast isolated from Roopkund Lake of the Himalayan mountain ranges, India. Extremophiles 12(3):375–381
Singer GA, Fasching C, Wilhelm L, Niggemann J, Steier P, Dittmar T, Battin TJ (2012) Biogeochemically diverse organic matter in Alpine glaciers and its downstream fate. Nat Geosci 5(10):710–714
Singh P, Singh SM (2012) Characterization of yeast and filamentous fungi isolated from cryoconite holes of Svalbard. Arctic Polar Biol 35(4):575–583
Smith HJ, Schmit A, Foster R, Littman S, Kuypers MM, Foreman CM (2016) Biofilms on glacial surfaces: hotspots for biological activity. NPJ Biofilms Microbiomes 2(1):1–4
Steedman HF (1950) Alcian blue 8GS: a new stain for mucin. J Cell Sci 3(16):477–479
Stibal M, Šabacká M, Žárský J (2012) Biological processes on glacier and ice sheet surfaces. Nat Geosci 5(11):771–774
Takeuchi N, Kohshima S, Seko K (2001) Structure, formation, and darkening process of albedo-reducing material (cryoconite) on a Himalayan glacier: a granular algal mat growing on the glacier. Arct Antarct Alp Res 33(2):115–122
Telling J, Anesio AM, Tranter M, Stibal M, Hawkings J, Irvine‐Fynn T, et al (2012) Controls on the autochthonous production and respiration of organic matter in cryoconite holes on high Arctic glaciers. J Geophys Res Biogeo 117(G1)
Turchetti B, Buzzini P, Goretti M, Branda E, Diolaiuti G, D’Agata C, Smiraglia C, Vaughan-Martini A (2008) Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbiol Ecol 63(1):73–83
Turchetti B, Goretti M, Branda E, Diolaiuti G, D’Agata C, Smiraglia C, Buzzini P (2013) Influence of abiotic variables on culturable yeast diversity in two distinct Alpine glaciers. FEMS Microbiol Ecol 86(2):327–340
Uetake J, Yoshimura Y, Nagatsuka N, Kanda H (2012) Isolation of oligotrophic yeasts from supraglacial environments of different altitude on the Gulkana Glacier (Alaska). FEMS Microbiol Ecol 82(2):279–286
Vaz AB, Rosa LH, Vieira ML, Garcia VD, Brandão LR, Teixeira LC, Rosa CA (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 42(3):937–947
Vero S, Garmendia G, Martínez-Silveira A, Cavello I, Wisniewski M (2019) Yeast activities involved in carbon and nitrogen cycles in antarctica in the ecological role of micro-organisms in the Antarctic Environment Springer, Cham, pp 45–64
Vishniac HS (1993) The microbiology of Antarctic soils. Antarctic microbiology 297–341
Vishniac HS (2006) A multivariate analysis of soil yeasts isolated from a latitudinal gradient. Microb Ecol 52(1):90–103
Wei S, Cui H, Jiang Z, Liu H, He H, Fang N (2015) Biomineralization processes of calcite induced by bacteria isolated from marine sediments. Braz J Microbiol 46(2):455–464
White TJ, Bruns T, Lee SJWT, Taylor JL (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Prot Guide Methods Appl 18(1):315–322
Wünnemann B, Demske D, Tarasov P, Kotlia BS, Reinhardt C, Bloemendal J et al (2010) Hydrological evolution during the last 15 kyr in the Tso Kar lake basin (Ladakh, India), derived from geomorphological, sedimentological and palynological records. Quat Sci Rev 29(9–10):1138–1155
You C, Yao T, Xu B, Xu C, Zhao H, Song L (2016) Effects of sources, transport, and post depositional processes on levoglucosan records in southeastern Tibetan glaciers. J Geophys Res Atmos 121(14):8701–8711
Acknowledgements
We thank the Ministry of Earth Science (India) for funding this work under ‘PACER - Cryosphere and Climate’ project and the Director, NCPOR, for support. We acknowledge the help of Ashish Paiguinkar and Lavkush Patel for sample collection from Himalaya and Archana Dayal for field assistance in Antarctica. Additionally, we acknowledge the help provided by Ashish Paiguinkar for conducting the analysis using the total organic carbon analyzer and ion chromatography. Thanks to K. Mahalinganathan for preparation of maps for this study. We would like to thank to Dr. Rahul Mohan for extending the facility of polarizing bright field microscope. This is NCPOR contribution number J-76/2020-21.
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The study was funded by Ministry of Earth Science (India) under ‘PACER - Cryosphere and Climate’ project.
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The study was conceived by RA and AS. Samples used for this study was collected by RA. AS and PG conducted the wet lab analysis. AS and RA wrote the paper, with inputs from MT.
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Sanyal, A., Antony, R., Ganesan, P. et al. Metabolic activity and bioweathering properties of yeasts isolated from different supraglacial environments of Antarctica and Himalaya. Antonie van Leeuwenhoek 113, 2243–2258 (2020). https://doi.org/10.1007/s10482-020-01496-1
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DOI: https://doi.org/10.1007/s10482-020-01496-1