Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 14, 2016

First report of microorganisms of Caucasus glaciers (Georgia)

  • Nicoletta Makowska , Krzysztof Zawierucha EMAIL logo , Joanna Mokracka and Ryszard Koczura
From the journal Biologia

Abstract

Glaciers constitute freshwater reservoirs. They are the main contributors to sea level rise, play an important role in global carbon cycle and are the source of water for people. Despite extreme conditions, they are also a habitat for a number of cryophilic organisms. To fill the gap in the knowledge on the biota on glaciers in Caucasus, the aim of the study was to: (i) isolate and enumerate culturable heterotrophs; (ii) determine the number of coliforms and enterococci bacteria; and (iii) analyze total microbial 16S rRNA gene in cryoconite sediments, ice and gravel. The material was collected from two glaciers in Caucasus (Georgia, Svaneti region). Bacteria Aeromonas sp. and Pseudomonas sp. were found. The total number of culturable heterotrophic bacteria ranged from 0.2 × 101 colony forming units per mL in ice and gravel of the Chalaadi Glacier to 3.9 x 103 colony forming units per mL in a cryoconite sediments of the Adishi Glacier. The average number of 16S rRNA gene copies ranged from 5.3 × 105/g to 5.3 × 106/g in ice and gravel from Chalaadi Glacier and from 3.1 × 105/g to 1.5 × 107/g in a cryoconite of the Adishi Glacier. The 16S rRNA gene of five Pseudomonas sp. isolates was sequenced. Moreover, in the analyzed cryoconite material, a rare collembolan Gnathisotoma sp. was found, which constitutes the first record of springtails in cryoconite holes in the Northern hemisphere.

Acknowledgements

The authors would like to thank Dr. Arne Fjellberg for the identification of Collembola and other important information. Special thanks go to Mr. Maciej Wilk and Mr. Piotr Nawrocki for their help during sample collection. We would like to thank the anonymous reviewer for valuable comments that improved the manuscript. Moreover, we are grateful to Adam Nawrot (the forScience Foundation), who prepared the map of investigated area. KZ is a beneficiary of National Science Center scholarship for PhD No. 2015/16/T/NZ8/00017. The studies were partially supported by National Science Centre grant No. NCN 2013/11/N/NZ8/00597 to KZ.

References

Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.10.1016/S0022-2836(05)80360-2Search in Google Scholar

Anesio A.M., Hodson A., Fritz A., Psenner R. & Sattler B. 2009. High microbial activity on glaciers: importance to the global carbon cycle. Glob. Change Biol. 15: 955–960.10.1111/j.1365-2486.2008.01758.xSearch in Google Scholar

Anesio A.M. & Laybourn-Parry J. 2012. Glaciers and ice sheets as a biome. Trends Ecol. Evol. 4: 219–225.10.1016/j.tree.2011.09.012Search in Google Scholar PubMed

Barros J., Becerra J., González C. & Martínez M. 2013. Antibacterial metabolites synthesized by psychrotrophic bacteria isolated from cold-freshwater environments. Folia Microbiol. 58: 127–133.10.1007/s12223-012-0190-xSearch in Google Scholar PubMed

Bellas C.M., Anesio A.M., Telling J., Stibal M., Tranter M. & Davis S. 2013. Viral impacts on bacterial communities in Arctic cryoconite. Environ. Res. Lett. 8: 1–9.10.1088/1748-9326/8/4/045021Search in Google Scholar

Carnahan A.M. & Joseph S.W. 2005. Order XII. Aeromonadales. 2nd Edition, Volume 2 (The Proteobacteria), Part B (The Gammaproteobacteria), pp. 556–578. In: Garrity G.M., Brenner D.J., Krieg N.R. & Staley J.T. (eds), Bergey’s Manual of Systematic Bacteriology. Springer, New York.Search in Google Scholar

Christner B.C., Kvitko B.H. & Reeve J.N. 2003. Molecular identification of Bacteria and Eukarya inhabiting an Antarctic cryoconite hole. Extremophiles 7: 177–183.10.1007/s00792-002-0309-0Search in Google Scholar PubMed

Cook J., Edwards A., Takeuchi N. & Irvine-Fynn T. 2016. Cryoconite: the dark biological secret of the cryosphere. Prog. Phys. Geog. 40: 66–111.10.1177/0309133315616574Search in Google Scholar

Coulson S.J., Convey P., Aakra K., Aarvik L., Ávila-Jiménez M.L., Babenko A., Biersma E.M., Boström S., Brittain J.E., Carlsson A.M., Christoffersen K., De Smet W.H., Ekremj T., Fjellberg A., Füreder L., Gustafssonm D., Gwiazdowicz D.J., Hansen L.O., Holmstrup M., Hullé M., Kaczmarek Ł., Kolicka M., Kuklin V., Lakka H.K., Lebedeva N., Makarova O., Maraldo K., Melekhina E., Ødegaard F., Pilskog H.E., Simon J.C., Sohlenius B., Solhøy T., Søli G., Stur E., Tanasevitch A., Taskaeva A., Velle G., Zawierucha K. & Zmudczyńska-Skarbek K. 2014. The terrestrial and freshwater invertebrate biodiversity of the archipelagoes of the Barents Sea; Svalbard, Franz Josef Land and Novaya Zemlya. Soil Biol. Biochem. 68: 440–470.10.1016/j.soilbio.2013.10.006Search in Google Scholar

Edwards A. 2015. Coming in from the cold: potential microbial threats from the terrestrial cryosphere. Front. Earth Sci. 3: 1210.3389/feart.2015.00012Search in Google Scholar

Edwards A., Anesio A.M., Rassner S.M., Sattler B., Hubbard B., Perkins W.T., Young M. & Griffith G.W. 2011. Possible interactions between bacterial diversity, microbial activity and supraglacial hydrology of cryoconite holes in Svalbard. ISME J. 5: 150–160.10.1038/ismej.2010.100Search in Google Scholar PubMed PubMed Central

Edwards A., Mur L.A.J., Girdwood S.E., Anesio A.M., Stibal M., Rassner S.M.E., Hell K., Pachebat J.A., Post B., Bussell J.S., Cameron S.J.S., Griffith G.W., Hodson A.J. & Sattler B. 2014. Coupled cryoconite ecosystem structure-function relationships are revealed by comparing bacterial communities in alpine and Arctic glaciers. FEMS Microbiol. Ecol. 89: 222–237.10.1111/1574-6941.12283Search in Google Scholar PubMed

Edwards A., Pachebat J.A., Swain M., Hegarty M., Hodson A.J., Irvine-Fynn T.D.L., Rassner S.M.E. & Sattler B. 2013. A metagenomic snapshot of taxonomic and functional diversity in an alpine glacier cryoconite ecosystem. Environ. Res. Lett. 8: 1–11.10.1088/1748-9326/8/3/035003Search in Google Scholar

Fjellberg A. 2010. Cryophilic Isotomidae (Collembola) of the Northwestern Rocky Mountains, U.S.A. Zootaxa 2513: 27–49.10.11646/zootaxa.2513.1.2Search in Google Scholar

Grape M., Farra A., Kronvall G. & Sundström L. 2005. Integrons and gene cassettes in clinical isolates of co-trimoxazole-resistant Gram-negative bacteria. Clin. Microbiol. Infect. 11: 185–192.10.1111/j.1469-0691.2004.01059.xSearch in Google Scholar PubMed

Grzesiak J., Górniak D., Świątecki A., Aleksandrzak-Piekarczyk T., Szatraj K. & Zdanowski M.K. 2015. Microbial community development on the surface of Hans and Werenskiold Glaciers (Svalbard, Arctic): a comparison. Extremophiles 19: 885–897.10.1007/s00792-015-0764-zSearch in Google Scholar PubMed PubMed Central

Gobejishvili R., Lomidze N. & Tielidze L. 2011. Late Pleistocene (Würmian) glaciations of the Caucasus. Dev. Quat. Sci. 15: 141–147.10.1016/B978-0-444-53447-7.00012-XSearch in Google Scholar

Havelaar A.H. & Vonk M. 1988. The preparation of ampicillin dextrin agar for the enumeration of Aeromonas in water. Lett. Appl. Microbiol. 7: 169–171.10.1111/j.1472-765X.1988.tb01271.xSearch in Google Scholar

Hodson A., Anesio A.M., Tranter M., Fountain A., Osborn M., Priscu J., Laybourn-Parry J. & Sattler B. 2008. Glacial ecosystems. Ecol. Monogr. 78: 41–67.10.1890/07-0187.1Search in Google Scholar

Hodson A., Cameron K., Břggild C., Irvine-Fynn T., Langford H., Pearce D. & Banwart S. 2010. The structure, biological activity and biogeochemistry of cryoconite aggregates upon an Arctic valley glacier: Longyearbreen, Svalbard. J. Glaciol. 56: 349–362.10.3189/002214310791968403Search in Google Scholar

Ikner L.A., Toomey R.S., Nolan G., Neilson J.W., Pryor B.M. & Maier R.M. 2007. Culturable microbial diversity and the impact of tourism in Kartchner Caverns, Arizona. Microb. Ecol. 53: 30–42.10.1007/s00248-006-9135-8Search in Google Scholar PubMed

Kaser G., Juen I., Georges C., Gomez J. & Tamayo W. 2003. The impact of glaciers on the runoff and the reconstruction of mass balance history from hydrological data in the tropical Cordillera Blanca, Peru. J. Hydrol. 282: 130–144.10.1016/S0022-1694(03)00259-2Search in Google Scholar

Kaczmarek Ł., Jakubowska N., Celewicz-Gołdyn S. & Zawierucha K. 2016. Cryoconite holes microorganisms (algae, Archaea, bacteria, cyanobacteria, fungi, and Protista) - a review. Polar Rec. 52: 176–203.10.1017/S0032247415000637Search in Google Scholar

Kikuchi Y. 1994. Glaciella, a new genus of freshwater Canthocamptidae (Copepoda, Harpacticoida) from a glacier in Nepal, Himalayas. Hydrobiologia 292: 59–66.10.1007/978-94-017-1347-4_8Search in Google Scholar

Kohshima S. 1984. A novel cold tolerant insect found in a Himalayan glacier. Nature 310: 225–227.10.1038/310225a0Search in Google Scholar

Labbé D., Margesin R., Schinner F., Whyte L.G. & Greer C.W. 2007. Comparative phylogenetic analysis of microbial communities in pristine and hydrocarbon-contaminated Alpine soils. FEMS Microbiol. Ecol. 59: 466–475.10.1111/j.1574-6941.2006.00250.xSearch in Google Scholar

Lee M.Y., Kim S.Y., Jung J., Kim E.H., Cho K.H., Schinner F., Margesin R., Hong S.G. & Lee H.K. 2011. Cultured bacterial diversity and human impact on Alpine glacier cryoconite. J. Microbiol. 49: 355–362.10.1007/s12275-011-0232-0Search in Google Scholar

Nossa C.W., Oberdorf W.E., Yang L., Aas J.A., Paster B.J., Desantis T.Z., Brodie E.L., Malamud D., Poles M.A. & Pei Z. 2010. Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World J. Gastroenter. 16: 4135–4144.10.3748/wjg.v16.i33.4135Search in Google Scholar

Pace N.R. 1997. A molecular view of microbial diversity and the biosphere. Science 276: 734–740.10.1126/science.276.5313.734Search in Google Scholar

Porazinska D.L., Fountain A.G., Nylen T.H., Tranter M., Virginia R.A. & Wall D.H. 2004. The biodiversity and biogeochemistry of cryoconite holes from McMurdo Dry Valley glaciers, Antarctica. Arc. Antarct. Alp. Res. 36: 84–91.10.1657/1523-0430(2004)036[0084:TBABOC]2.0.CO;2Search in Google Scholar

Radić V., Bliss A., Beedlow A.C., Hock R., Miles E. & Cogley J.G. 2014. Regional and global projections of twenty-first century glacier mass changes in response to climate scenarios from global climate models. Clim. Dynam. 42: 37–58.10.1007/s00382-013-1719-7Search in Google Scholar

Saul D.J., Aislabie J.M., Brown C.E., Harris L. & Foght J.M. 2005. Hydrocarbon contamination changes the bacterial diversity of soil from around Scott Base, Antarctica. FEMS Microbiol. Ecol. 53: 141–155.10.1016/j.femsec.2004.11.007Search in Google Scholar

Säwström C., Mumford P., Marshall W., Hodson A. & Laybourn-Parry J. 2002. The microbial communities and primary productivity of cryoconite holes in an Arctic glacier (Svalbard 79° N). Polar Biol. 25: 591–596.10.1007/s00300-002-0388-5Search in Google Scholar

Segawa T., Yoshimura Y., Watanabe K., Kanda H. & Kohshima S. 2011. Community structure of culturable bacteria on surface of Gulkana Glacier, Alaska. Polar Sci. 5: 41–51.10.1016/j.polar.2010.12.002Search in Google Scholar

Sheridan P.P., Miteva V.I. & Brenchley J.E. 2003. Phylogenetic analysis of anaerobic psychrophilic enrichment cultures obtained from a Greenland glacier ice core. Appl. Environ. Microbiol. 69: 2153–2160.10.1128/AEM.69.4.2153-2160.2003Search in Google Scholar

Singh P., Singh S.M. & Dhakephalkar P. 2014. Diversity, cold active enzymes and adaptation strategies of bacteria inhabiting glacier cryoconite holes of High Arctic. Extremophiles 18: 229–242.10.1007/s00792-013-0609-6Search in Google Scholar

Smith C.J. & Osborn A.M. 2009. Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiol. Ecol. 67: 6–20.10.1111/j.1574-6941.2008.00629.xSearch in Google Scholar

Stibal M., Schostag M., Cameron K.A., Hansen L.H., Chandler D.M., Wadham J.L. & Jacobsen C.S. 2015. Different bulk and active bacterial communities in cryoconite from the margin and interior of the Greenland ice sheet. Environ. Microbiol. Rep. 7: 293–300.10.1111/1758-2229.12246Search in Google Scholar

Takeuchi N. & Kohshima S. 2004. A snow algal community on Tyndall Glacier in the Southern Patagonia Icefield, Chile. Arct. Antarct. Alp. Res. 36: 92–99.10.1657/1523-0430(2004)036[0092:ASACOT]2.0.CO;2Search in Google Scholar

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. Arc. Antarct. Alp. Res. 33: 115–122.10.1080/15230430.2001.12003413Search in Google Scholar

Tielidze L.G., Lominadze G. & Lomidze N. 2015. Glaciers fluctuation over the last half century in the headwaters of the Enguri River, Caucasus Mountains, Georgia. Int. J. Geosci. 6: 393–401.10.4236/ijg.2015.64031Search in Google Scholar

Vaughan D.G., Comiso J.C., Allison I., Carrasco J., Kaser G., Mote P., Murray T., Paul F., Ren J., Rignot E., Solomina O., Steffen K. & Zhang T. 2013. Observations: Cryosphere. In: Stocker T.F., Qin D., Plattner G.K., Tignor M., Allen S.K. & Boschung J. (eds), Contribution of working group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.Search in Google Scholar

Webster N.S. & Negri A. P. 2006. Site-specific variation in Antarctic marine biofilms established on artificial surfaces. Environ. Microbiol. 8: 1177–1190.10.1111/j.1462-2920.2006.01007.xSearch in Google Scholar PubMed

Wharton R.A., McKay C.P., Simmons G.M. & Parker B.C. 1985. Cryoconite holes on glaciers. Bioscience 35: 499–503.10.2307/1309818Search in Google Scholar

Xi C., Zhang Y., Marrs Y.L., Ye W., Simon C., Foxman B. & Nriagu J. 2009. Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Appl. Environ. Microbiol. 75: 5714–5718.10.1128/AEM.00382-09Search in Google Scholar PubMed PubMed Central

Zawierucha K., Kolicka M., Takeuchi N. & Kaczmarek Ł. 2015. What animals can live in cryoconite holes? A faunal review. J. Zool. 295: 159–169.10.1111/jzo.12195Search in Google Scholar

Zawierucha K., Vonnahme T.R., Devetter M., Kolicka M., Ostrowska M., Chmielewski S. & Kosicki J.Z. 2016. Area, depth and elevation of cryoconite holes in the Arctic do not influence Tardigrada densities. Pol. Polar Res. 37: 325–334.10.1515/popore-2016-0009Search in Google Scholar

Zhang S.H., Hou S.G., Yang G.L., Wang J.H. 2010. Bacterial community in the East Rongbuk Glacier, Mt. Qomolangma (Everest) by culture and culture-independent methods. Microbiol. Res. 165: 336–345.10.1016/j.micres.2009.08.002Search in Google Scholar PubMed

Zhang W., Zhang G., Liu G., Li Z., Chen T. & An L. 2012. Diversity of bacterial communities in the snowcover at tian shan number 1 glacier and its relation to climate and environment. Geomicrobiol. J. 29: 459–469.10.1080/01490451.2011.581329Search in Google Scholar

Abbreviations
asl

above sea level

CFU

colony forming units

qPCR

quantitative real-time PCR.

Received: 2016-3-25
Accepted: 2016-6-8
Published Online: 2016-7-14
Published in Print: 2016-6-1

©2016 Institute of Molecular Biology, Slovak Academy of Sciences

Downloaded on 4.6.2023 from https://www.degruyter.com/document/doi/10.1515/biolog-2016-0086/html
Scroll to top button