Skip to main content
Log in

Thermokarst Lakes, Ecosystems with Intense Microbial Processes of the Methane Cycle

  • REVIEWS
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Thermokarst lakes are formed as a result of thawing of ice-rich permafrost, causing development of land depressions which in flat areas are filled with water in the case of positive water balance. Activation of the thermokarst process is one of the possible indicators of permafrost degradation under the conditions of global warming. Thermokarst lakes occur in the areas of continuous, discontinuous, and sporadic permafrost, i.e., in Siberia, Alaska, Canada, and northern Scandinavia. Specific microbial communities adapted to long-term exposure to low temperatures develop in such lakes. They vary in the rates of aerobic and anaerobic metabolism depending on the mineral composition of bottom sediments, availability of organic matter, limnological and hydrological features of the lakes. High rates of methane emission are characteristic of a number of thermokarst lakes. Recent studies of thermokarst lakes revealed active methane formation via various methanogenic pathways, as well as aerobic and anaerobic methane oxidation by diverse methanogenic and methanotrophic bacteria and archaea. The question of what mechanisms and microorganisms are involved in anaerobic methane oxidation, which may be responsible for up to 80% of methane consumption in thermokarst lakes, remains, however, open. The microorganisms actively functioning beneath the ice during the long winter season, while highly important for northern aquatic ecosystems, also remain insufficiently studied. Almost no serious microbiological research on thermokarst lakes has been carried out in Russia, although permafrost occupies up to 65% of its territory, thermokarst process is common, and thermokarst lakes are numerous.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. Boitsov, A.V., Geokriologiya i podzemnye vody kriolitozony (Geocryology and Cryolithozone Groundwaters), Tyumen: TyumGNGU, 2011.

  2. Borrel, G., Jézéquel, D. Biderre-Petit, C., Morel-Desrosiers, N., Morel, J. P., Peyret, P., Fonty, G., and Lehours, A.C., Production and consumption of methane in freshwater lake ecosystems, Res. Microbiol., 2011, vol. 162, pp. 832‒847.

    Article  CAS  PubMed  Google Scholar 

  3. Bouchard, F., MacDonald, L.A., Turner, K.W., Thienpont, J.R., Medeiros, A.S., Biskaborn, B.K., Korosi, J., Hall, R.I., Pienitz, R., and Wolfe, B.B., Paleolimnology of thermokarst lakes: a window into permafrost landscape evolution, Arctic Sci., 2017, vol. 3, pp. 91–117.

    Article  Google Scholar 

  4. Bryksina, N.A., Evtyushkin, A.V., and Polishchuk, Yu.M., Investigation of dynamics of the changes in thermokarst relief forms using space photography, Curr. Probl. Remote Sens.Earth from Space, 2007, vol. 4., no. 2, pp. 123‒128.

    Google Scholar 

  5. Bryksina, N.A., Polishchuk, V.Yu., and Polischshuk, Yu.M., Database of Western Siberian thermokarst lakes based on space photographs and the possibilities for its practical application Curr. Probl. Remote Sens.Earth from Space, 2011, vol. 8., no. 3, pp. 175‒181.

    Google Scholar 

  6. Calmels, F., Allard, M., and Delisle, G., Development and decay of a lithalsa in northern Quebec: a geomorphological history, Geomorphology, 2008, vol. 97, pp. 287–299.

    Article  Google Scholar 

  7. Chistoserdova, L., Methylotrophs in natural habitats: current insights through metagenomics, Appl. Microbiol. Biotechnol., 2015, vol. 99, pp. 5763‒5779.

    Article  CAS  PubMed  Google Scholar 

  8. Ciais, P., Sabine, C., Bala, G., Bopp, L., Brovkin, V., Canadell, J., Chhabra, A., DeFries, R., Galloway, J., Heimann, M., Jones, C., Le Quéré, C., Myneni, R.B., Piao, S., and Thornton, P., Carbon and other biogeochemical cycles, in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V., and Midgley, P.M., Eds., Cambridge: Cambridge Univ. Press, 2013, pp. 465‒570.

    Google Scholar 

  9. Crate, S., Ulrich, M., Habeck, J.O., Desyatkin, A.R., Desyatkin, R.V., Fedorov, A.N., Hiyama, T., Iijima, Y., Ksenofontov, S., Mészáros, C., and Takakura, H., Permafrost livelihoods: a transdisciplinary review and analysis of thermokarst-based systems of indigenous land use, Anthropocene, 2017, vol. 18, pp. 89–104.

    Article  Google Scholar 

  10. Crevecoeur, S., Vincent, W.F., Comte, J., and Lovejoy, C., Bacterial community structure across environmental gradients in permafrost thaw ponds: methanotroph-rich ecosystems, Front. Microbiol., 2015, vol. 6. 192. https://doi.org/10.3389/fmicb.2015.00192

    Article  PubMed  PubMed Central  Google Scholar 

  11. Crevecoeur, S., Vincent, W.F., Comte, J., Matveev, A., and Lovejoy, C., Diversity and potential activity of methanotrophs in high methane-emitting permafrost thaw ponds, PLoS One, 2017, vol. 12. e0188223.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Crump, B.C., Amaral-Zettler, L.A., and Kling, G.W., Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils, ISME J., 2012, vol. 6, pp. 1629–1639.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. de Jong, A.E.E., In’t Zandt, M.H., Meisel, O.H., Jetten, M.S.M., Dean, J.F., Rasigraf, O., and Welte, C.U., Increases in temperature and nutrient availability positively affect methane-cycling microorganisms in Arctic thermokarst lake sediments, Environ. Microbiol., 2018, vol. 20, pp. 4314‒4327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Drozdov, D.S., Malkova, G.V., Romanovsky, V.E., Rumyantseva, Ya.V., Abramov, A.A., Konstantinov, P.Ya., Sergeev, D.O., Shiklomanov, N.I., Kholodov, A.L., Ponomareva, O.E., and Streletskiy, D.A., Monitoring of permafrost in Russia. Russian database and the international GTN-P project, Proc. 68th Canad. Geotech. Conf., Quebec, 2015.

  15. Dumont, M.G, Lüke, C., Deng, Y., and Frenzel, P., Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGAN, Front Microbiol., 2014, vol. 5. 34. https://doi.org/10.3389/fmicb.2014.00034

    Article  PubMed Central  Google Scholar 

  16. Efimov, A.I., On development of thermokarst lakes in Central Yakutiya, in Issledovanie vechnoi merzloty v Yakutskoi respublike (Premafrost Research in Yakut Republic), Moscow: AN SSSR, 1950, no. 2, pp. 98–114.

    Google Scholar 

  17. Egger, M., Rasigraf, O., Sapart, C.J., Jilbert, T., Jetten, M.S., Röckmann, T., van der Veen, C., Bândă, N., Kartal, B., Ettwig, K.F., and Slomp, C.P., Iron-mediated anaerobic oxidation of methane in brackish coastal sediments, Environ. Sci. Technol., 2015, vol. 49, pp. 277‒283.

    Article  CAS  PubMed  Google Scholar 

  18. Elder, C.D., Xu, X., Walker, J., Schnell, J.L., Hinkel, K.M., Townsend-Small, A., Arp, C.D., Pohlman, J.W., Gaglioti, B.V., and Czimczik, C.I., Greenhouse gas emissions from diverse Arctic Alaskan lakes are dominated by young carbon, Nature Climate Change, 2018, vol. 8, pp. 166–171.

    Article  CAS  Google Scholar 

  19. Ettwig, K.F., Zhu, B., Speth, D., Keltjens, J.T., Jetten, M.S.M., and Kartal, B., Archaea catalyze iron-dependent anaerobic oxidation of methane, Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, pp. 12792–12796.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Fu, L., Li, S.W., Ding, Z.W., Ding, J., Lu, Y.Z., and Zeng, R.J., Iron reduction in the DAMO/Shewanella oneidensis MR-1 coculture system and the fate of Fe(II), Water Res., 2016, vol. 88, pp. 808‒815.

    Article  CAS  PubMed  Google Scholar 

  21. Gilichinsky, D.A., Wagener, S., and Vishnevetskaya, T.A., Permafrost microbiology, Permafrost Periglacial Proc., 1995, vol. 6, pp. 281‒291.

    Article  Google Scholar 

  22. Graf, J.S., Mayr, M.J., Marchant, H.K., Tienken, D., Hach, P.F., Brand, A., Schubert, C.J., Kuypers, M.M.M., and Milucka, J., Bloom of a denitrifying methanotroph, “Candidatus Methylomirabilis limnetica”, in a deep stratified lake, Environ. Microbiol., 2018, vol. 20, pp. 2598‒2614.

    Article  CAS  PubMed  Google Scholar 

  23. Grosse, G., Jones, B., and Arp, C., Thermokarst lakes, drainage, and drained basins, in Treatise on Geomorphology, Shroder, J.F., Ed., San Diego: Academic, 2013, pp. 325–353.

    Google Scholar 

  24. Hanson, R.S. and Hanson, T.E., Methanotrophic bacteria, Microbiol. Rev., 1996, vol. 60, pp. 439‒471.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. He, R., Wooller, M.J., Pohlman, J.W., Quensen, J., Tiedje, J.M., and Leigh, M.B., Shifts in identity and activity of methanotrophs in arctic lake sediments in response to temperature changes, Appl. Environ. Microbiol., 2012, vol. 78, pp. 4715‒4723.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Heslop, J.K., Walter Anthony, K.M., Sepulveda-Jauregui, A., Martinez-Cruz, K., Bondurant, A., Grosse, G., and Jones, M.C., Thermokarst lake methanogenesis along a complete talik profile, Biogeosci., 2015, vol. 12, pp. 4317–4331.

    Article  Google Scholar 

  27. He, Z., Zhang, Q., Feng, Y., Luo, H., Pan, X., Gadd, G.M., Microbiological and environmental significance of metal-dependent anaerobic oxidation of methane, Sci. Total Environ., 2018, vol. 610‒611, pp. 759‒768.

    Article  CAS  Google Scholar 

  28. Hjort, J., Karjalainen, O., Aalto, J., Westermann, S., Romanovsky, V.E., Nelson, F.E., Etzelmüller, B., and Luoto, M., Degrading permafrost puts Arctic infrastructure at risk by mid-century, Nat. Commun., 2018, vol. 9. 5147. https://doi.org/10.1038/s41467-018-07557-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jorgenson, M.T., Racine, C.H., Walters, J.C., and Osterkamp, T.E., Permafrost degradation and ecological changes associated with a warming climate in Central Alaska, Climatic Change, 2001, vol. 48, pp. 551‒579.

    Article  CAS  Google Scholar 

  30. Kachurin, S.P., Termokarst na territorii SSSR (Thermokarst on the USSR Territory), AN SSSR, 1961.

  31. Kallistova, A., Kadnikov, V., Rusanov, I., Kokryatskaya, N., Beletsky, A., Mardanov, A., Savvichev, A., Ravin, N., and Pimenov, N., Microbial communities involved in aerobic and anaerobic methane cycling in a meromictic ferruginous subarctic lake, Aquat. Microb. Ecol., 2019, vol. 82, pp. 1‒18.

    Article  Google Scholar 

  32. Kallistova, A.Yu., Merkel, A.Yu., Tarnovetskii, I.Yu., and Pimenov, N.V., Methane formation and oxidation by prokaryotes, Microbiology (Moscow), 2017, vol. 86, pp. 671‒691.

    Article  CAS  Google Scholar 

  33. Kravtsova, V.I. and Rodionova, T.V., Variations in size and number of thermokarst lakes in different permafrost regions: spaceborne evidence, Earth’s Cryosphere, 2016, vol. 20, pp. 75‒81.

    Google Scholar 

  34. Kravtsova, V.I. and Tarasenko, T.V., Dynamics of thermokarst lakes in Central Yakutiya during climatic changes after 1950, Kriosfera Zemli, 2011, vol. 15, no. 3, pp. 31‒42.

    Google Scholar 

  35. Kravtsova, V.I., Occurrence of thermokarst lakes in Russia, Vestn. Mos. Univ. Ser. Geogr., 2009, no. 3, pp. 33‒42.

  36. Laurion, I., Vincent, W.F., MacIntyre, S., Retamal, L., Dupont, C., Francus, P., and Pienitz, R., Variability in greenhouse gas emissions from permafrost thaw ponds, Limnol. Oceanogr., 2010, vol. 55, pp. 115‒133.

    Article  CAS  Google Scholar 

  37. Lawrence, D.M. and Slater, A.G., A projection of severe near-surface permafrost degradation during the 21st century, Geophys. Res. Let., 2005, vol. 32. L24401. https://doi.org/10.1029/2005GL025080

    Article  Google Scholar 

  38. Leibman, M.O., Arkhipov, S.M., Perednya, D.D., Savvichev, A.S., Vanshtein, B.G., and Hubberten, H.-W., Geochemical properties of the water–snow–ice complexes in the area of Shokalsky glacier, Novaya Zemlya, in relation to tabular ground-ice formation, Ann. Glaciol., 2005, vol. 42, pp. 249‒254.

    Article  CAS  Google Scholar 

  39. Leibman, M.O., Kizyakov, A.I., Plekhanov, A.V., and Streletskaya, I.D., New permafrost feature—deep crater in Central Yamal (West Siberia, Russia) as a response to local climate fluctuations, Geography, Environment,Sustainability, 2014, vol. 7, pp. 68‒79.

    Google Scholar 

  40. Lein, A.Yu., Leibman, M.O., Savvichev, A.S., Miller, Yu.M., and Pimenov, N.V., Isotopic and biogeochemical characteristics of tabular ground ice on the Yugorskii and Yamal peninsulas, Geochem. Int., 2003, vol. 41, pp. 993‒1012.

    Google Scholar 

  41. Lein, A.Yu., Savvichev, A.S., Leibman, M.O., and Perednya, D.D., Ice record: example of decryption using isotope tracers, Priroda, 2005, no. 7, pp. 25‒34.

  42. Lidström, M.E. and Somers, L., Seasonal study of methane oxidation in Lake Washington, Appl. Environ. Microbiol., 1984, vol. 47, pp. 1255–1260.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Martinez-Cruz, K., Leewis, M.C., Herriott, I.C., Sepulveda-Jauregui, A., Walter Anthony, K., Thalasso, F., and Leigh, M.B., Anaerobic oxidation of methane by aerobic methanotrophs in sub-Arctic lake sediments, Sci. Total Environ., 2017, vols. 607‒608, pp. 23‒31.

    Article  CAS  Google Scholar 

  44. Martinez-Cruz, K., Sepulveda-Jauregui, A., Casper, P., Walter Anthony, K., Smemo, K.A., and Thalasso, F., Ubiquitous and significant anaerobic oxidation of methane in freshwater lake sediments, Water Res., 2018, vol. 144, pp. 332‒340.

    Article  CAS  PubMed  Google Scholar 

  45. Martinez-Cruz, K., Sepulveda-Jauregui, A., Walter Anthony, K., and Thalasso, F., Geographic and seasonal variation of dissolved methane and aerobic methane oxidation in Alaskan lakes, Biogeosci., 2015, vol. 12, pp. 4595–4606.

    Article  Google Scholar 

  46. Matheus Carnevali, P.B., Herbold, C.W., Hand, K.P., Priscu, J.C., and Murray, A.E., Distinct microbial assemblage structure and archaeal diversity in sediments of Arctic thermokarst lakes differing in methane sources, Front. Microbiol., 2018, vol. 9. 1192. https://doi.org/10.3389/fmicb.2018.01192

    Article  PubMed  PubMed Central  Google Scholar 

  47. Matheus Carnevali, P.B., Rohrssen, M., Williams, M.R., Michaud, A.B., Adams, H., Berisford, D., Love, G.D., Priscu, J.C., Rassuchine, O., Hand, K.P., and Murray, A.E., Methane sources in arctic thermokarst lake sediments on the North Slope of Alaska, Geobiology, 2015, vol. 13, pp. 181‒197.

    Article  CAS  PubMed  Google Scholar 

  48. McGlynn, S.E., Energy metabolism during anaerobic methane oxidation in ANME archaea, Microbes Environ., 2017, vol. 32, pp. 5‒13.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Mondav, R., Woodcroft, B.J., Kim, E.-H., McCalley, C.K., Hodgkins, S.B., Crill, P.M., Chanton, J., Hurst, G.B., VerBerkmoes, N.C., Saleska, S.R., Hugenholtz, P., Rich, V.I., and Tyson, G.W., Discovery of a novel methanogen prevalent in thawing permafrost, Nat. Commun., 2014, vol. 5. 3212. https://doi.org/10.1038/ncomms4212

    Article  CAS  PubMed  Google Scholar 

  50. Negandhi, K., Laurion, I., and Lovejoy C., Bacterial communities and greenhouse gas emissions of shallow ponds in the High Arctic, Polar Biol., 2014, vol. 37, pp. 1669–1683.

    Article  Google Scholar 

  51. Negandhi, K., Laurion, I., and Lovejoy C., Temperature effects on net greenhouse gas production and bacterial communities in arctic thaw ponds, FEMS Microbiol. Ecol., 2016, vol. 92. fiw117.

    Article  PubMed  CAS  Google Scholar 

  52. Negandhi, K., Laurion, I., Whiticar, M.J., Galand, P.E., Xu, X., and Lovejoy, C., Small thaw ponds: an unaccounted source of methane in the Canadian High Arctic, PLoS One, 2013, vol. 8. e78204.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Obshchee merzlotovedetie (General Permafrost Science), Kudryavtsev, V.A., Ed., Moscow: Mos. Gos. Univ., 1978.

    Google Scholar 

  54. Oliva, M. and Fritz, M., Permafrost degradation on a warmer Earth: Challenges and perspectives, Curr. Opin. Environ. Sci. Health, 2018, vol. 5, pp. 14‒18.

    Article  Google Scholar 

  55. Osudar, R., Liebner, S., Alawi, M., Yang, S., Bussmann, I., and Wagner, D., Methane turnover and methanotrophic communities in arctic aquatic ecosystems of the Lena Delta, Northeast Siberia, FEMS Microbiol. Ecol., 2016, vol. 92. fiw116.

    Article  PubMed  CAS  Google Scholar 

  56. Oswald, K., Graf, J.S., Littmann, S., Tienken, D., Brand, A., Wehrli, B., Albertsen, M., Daims, H., Wagner, M., Kuy-pers, M.M., Schubert, C.J., and Milucka, J., Crenothrix are major methane consumers in stratified lakes, ISME J., 2017, vol. 11, pp. 2124−2140.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Oswald, K., Milucka, J., Brand, A., Hach, P., Littmann, S., Wehrli, B., Kuypers, M.M., and Schubert, C.J., Aerobic gammaproteobacterial methanotrophs mitigate methane emissions from oxic and anoxic lake waters, Limnol. Oceanogr., 2016, vol. 61, pp. S101–S118.

    Article  CAS  Google Scholar 

  58. Payette, S., Delwaide, A., Caccianiga, M., and Beauchemin, M. Accelerated thawing of subarctic peatland permafrost over the last 50 years, Geophys. Res. Lett., 2004, vol. 31. L18208.

    Article  Google Scholar 

  59. Pokrovskii, O.S., Shirokova, L.S., and Kirpotin, S.N., Microbiological factors controlling the carbon cycle in thermokarst water objects of Western Siberia, Vestn. Tomsk. Univ. Biol., 2012, no. 3 (19), pp. 199–217.

  60. Polishchyuk, Yu.M., Bryksina, N.A., and Kupriyanov, M.A., Comparative analysis of changes in lake size in the Western and Eastern Siberian permafrost zone using space photographs, Geoinformatika, 2016, no. 1, pp. 64‒67.

  61. Polishchyuk, Yu.M., Kupriyanov, M.A., and Bryksina, N.A., Remote investigation of lake dynamics and ares in the continuous cryolithozone of Siberia, Geogr. Prirod. Res., 2017, no. 3, pp. 164‒170.

  62. Popov, A.I., Rozenbaum, G.E., and Tumel’, N.V., Kriolitologiya: uchebnoe posobie (Cryolithology: A Tutorial), Moscow: Mos. Gos. Univ., 1985.

  63. Rissanen, A.J., Saarenheimo, J., Tiirola, M., Peura, S., Aalto, S.L., Karvinen, A., and Nykänen, H., Gammaproteobacterial methanotrophs dominate methanotrophy in aerobic and anaerobic layers of boreal lake waters, Aquat. Microb. Ecol., 2018, vol. 81, pp. 257‒276.

    Article  Google Scholar 

  64. Rivkina, E., Laurinavichius, K., McGrath, J., Tiedje, J., Shcherbakova, V., and Gilichinsky, D., Microbial life in permafrost, Adv. Space Res., 2004, vol. 33, pp. 1215–1221.

    Article  CAS  PubMed  Google Scholar 

  65. Rivkina, E.M., Kraev, G.N., Krivushin, K.V., Laurinavichyus, K.S., Fedorov-Davydov, D.G., Kholodov, A.L., Shcherbakova, V.A., and Gilichinskii, D.A., Methane in permafrost deposits of the Northeastern Arctic sector, Kriosfera Zemli, 2006, vol. 10, no. 3, pp. 23–41.

    Google Scholar 

  66. Rodionova, T.V., Investigation of dynamics of thermokarst lakes in various regions of the Russian cryolithozone using spece photography, Cand. Sci. (Geogr.) Dissertation, Moscow, 2013.

  67. Romanovskii, N.N., Osnovy kriogeneza litosfery (Basics of Lithospheric Cryogenesis), Moscow: Mos. Gos. Univ., 1993.

  68. Romanovskii, N.N., Podzemnye vody kriolitozony (Subsurface Waters of the Cryolithozone), Moscow: Mos. Gos. Univ., 1983.

  69. Romanovsky, V., Isaksen, K., Drozdov, D., Anisimov, O., Instanes, A., Leibman, M., McGuire, A.D., Shiklomanov, N., Smith, S., and Walker, D., Changing permafrost and its impacts, Snow, Water, Ice and Permafrost in the Arctic (SWIPA), Oslo: AMAP, 2017, pp. 65‒102.

    Google Scholar 

  70. Saunois, M., Bousquet, P., Poulter, B., Peregon, A., Ciais, P., Canadell, J.G., Dlugokencky, E.J., Etiope, G., Bastviken, D., Houweling, S., Janssens-Maenhout, G., Tubiello, F.N., Castaldi, S., Jackson, R.B., Alexe, M., et al., The global methane budget 2000–2012, Earth. Syst. Sci. Data, 2016, vol. 8, pp. 697–751.

    Article  Google Scholar 

  71. Savvichev, A., Leibman, M., Kadnikov, V., Kallistova, A., Pimenov, N., Ravin, N., Dvornikov, Y., and Khomutov, A., Microbiological study of Yamal lakes: a key to understanding the evolution of gas emission craters, Geosci., 2018, vol. 8. 478. https://doi.org/10.3390/geosciences8120478

    Article  CAS  Google Scholar 

  72. Sepulveda-Jauregui, A., Walter Anthony, K.M., Martinez-Cruz, K., Greene, S., and Thalasso, F., Methane and carbon dioxide emissions from 40 lakes along a north–south latitudinal transect in Alaska, Biogeosci., 2015, vol. 12, pp. 3197‒3223.

    Article  CAS  Google Scholar 

  73. Serikova, S., Pokrovsky, O.S., Laudon, H., Krickov, I.V., Lim, A.G., Manasypov, R.M., and Karlsson, J., High carbon emissions from thermokarst lakes of Western Siberia, Nat. Commun., 2019, vol. 10. 1552. https://doi.org/10.1038/s41467-019-09592-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Shcherbakova, V., Rivkina, E., Laurinavichuis, K., Pecheritsina, S., and Gilichinsky, D., Physiological characteristics of bacteria isolated from water brines within permafrost, Int. J. Astrobiol., 2004, vol. 3, pp. 37–43.

    Article  CAS  Google Scholar 

  75. Shcherbakova, V., Yoshimura, Y., Ryzhmanova, Y., Taguchi, Y., Segawa, T., Oshurkova, V., and Rivkina, E., Archaeal communities of Arctic methane-containing permafrost, FEMS Microbiol. Ecol., 2016, vol. 92. fiw135.

    Article  PubMed  CAS  Google Scholar 

  76. Shirokova, L.S., Pokrovsky, O.S., Kirpotin, S.N., Desmukh, C., Pokrovsky, B.G., Audry, S., and Viers, J., Biogeochemistry of organic carbon, CO2, CH4, and trace elements in thermokarst water bodies in discontinuous permafrost zones of Western Siberia, Biogeochemistry, 2013, vol. 113, pp. 573–593.

    Article  CAS  Google Scholar 

  77. Singleton, C.M., McCalley, C.K., Woodcroft, B.J., Boyd, J.A., Evans, P.N., Hodgkins, S.B., Chanton, J.P., Frolking, S., Crill, P.M., Saleska, S.R., Rich, V.I., and Tyson, G.W., Methanotrophy across a natural permafrost thaw environment, ISME J., 2018, vol. 12, pp. 2544‒2558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Solov’ev, P.A., Alas relief in Central Yakutiya and its origin, in Mnogoletnemerzlye porody i soputstvuyushchie im yavleniya na territorii Yakutskoi ASSR (Permafrost and Accompanying Phenomena in Yakut ASSR), Moscow: AN SSSR, 1962, pp. 38–53.

  79. Sumgin, M.I., Vechnaya merzlota pochvy v predelakh SSSR (Soil Premafrost in USSR), Vladivostok: NKZ, 1927. http://books.e-heritage.ru/book/10080861.

  80. Timmers, P.H., Welte, C.U., Koehorst, J.J., Plugge, C.M., Jetten, M.S., and Stams, A.J., Reverse methanogenesis and respiration in methanotrophic archaea, Archaea, 2017. https://doi.org/10.1155/2017/1654237

  81. Townsend-Small, A., Åkerström, F., Arp, C.D., and Hinkel, K.M., Spatial and temporal variation in methane concentrations, fluxes, and sources in lakes in Arctic Alaska, J. Geophys. Res: Biogeosci., 2017, vol. 122, pp. 2966–2981.

    Article  CAS  Google Scholar 

  82. Vonk, J.E., Tank, S.E., Bowden, W.B., Laurion, I., Vincent, W.F., Alekseychik, P., Amyot, M., Billet, M.F., Canário, J., Cory, R.M., Deshpande, B.N., Helbig, M., Jammet, M., Karlsson, J., Larouche, J., et al., Reviews and syntheses: effects of permafrost thaw on Arctic aquatic ecosystems, Biogeosciences, 2015, vol. 12, pp. 7129–7167.

    Article  CAS  Google Scholar 

  83. Walter Anthony, K.M., Zimov, S.A., Grosse, G., Jones, M.C., Anthony, P.M., Chapin, F.S., Finlay, J.C., Mack, M.C., Davydov, S., Frenzel, P., and Frolking, S., A shift of thermokarst lakes from carbon sources to sinks during the Holocene epoch, Nature, 2014, vol. 511, pp. 452–456.

    Article  CAS  Google Scholar 

  84. Walter, K.M., Smith, L.C., and Chapin, F.S., Methane bubbling from northern lakes: present and future contributions to the global methane budge, Philos. Trans. A Math.Phys. Eng. Sci., 2007, vol. 365, pp. 1657‒1676.

    Article  CAS  Google Scholar 

  85. Walter, K.M., Zimov, S.A., Chanton, J.P., Verbyla, D., and Chapin, F.S., Methane bubbling from Siberian thaw lakes as a positive feedback to climate warming, Nature, 2006, vol. 443, pp. 71–75.

    Article  CAS  PubMed  Google Scholar 

  86. Wei, S., Cui, H., Zhu, Y., Lu, Z., Pang, S., Zhang, S., Dong, H., and Su, X., Shifts of methanogenic communities in response to permafrost thaw results in rising methane emissions and soil property changes, Extremophiles, 2018, vol. 22, pp. 447‒459.

    Article  CAS  PubMed  Google Scholar 

  87. Welte, C.U., Rasigraf, O., Vaksmaa, A., Versantvoort, W., Arshad, A., Op den Camp, H.J., Jetten, M.S., Lüke, C., and Reimann, J., Nitrate- and nitrite-dependent anaerobic oxidation of methane, Environ. Microbiol. Rep., 2016, vol. 8, pp. 941‒955.

    Article  CAS  PubMed  Google Scholar 

  88. Wik, M., Varner, R.K., Walter Anthony, K., MacIntyre, S., and Bastviken, D. Climate-sensitive northern lakes and ponds are critical components of methane release, Nat. Geosci., 2016, vol. 9, pp. 99‒105.

    Article  CAS  Google Scholar 

  89. Winkel, M., Sepulveda-Jauregui, A., Martinez-Cruz, K., Heslop, J.K., Rijkers, R., Horn, F., Liebner, S., and Walter Anthony, K.M., First evidence for cold-adapted anaerobic oxidation of methane in deep sediments of thermokarst lakes, Environ. Res. Commun., 2019, vol. 1. 021002.

    Article  Google Scholar 

  90. Zabelina, S.A., Shirokova, L.S., Kovalev, O.D., Chupakov, A.V., and Chupakova, A.A., Bacterioplankton structure in thermokarst lakes of Bol’shezemel’skaya Tundra, Trudy IBVV RAN, 2017, no. 79 (82), pp. 58‒62.

  91. Zimov, S.A., Schuur, E.A.G., and Chapin, F.S., Permafrost and the global carbon budget, Science, 2006, vol. 312, pp. 1612–1613.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was supported by the Russian Science Foundation, project no. 16-14-10201; the work of I.I. Rusanov was supported by the Russian Federation Ministry of Science and Higher Education.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Yu. Kallistova.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kallistova, A.Y., Savvichev, A.S., Rusanov, I.I. et al. Thermokarst Lakes, Ecosystems with Intense Microbial Processes of the Methane Cycle. Microbiology 88, 649–661 (2019). https://doi.org/10.1134/S0026261719060043

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261719060043

Keywords:

Navigation