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Variability of Microbial Communities in Two Long-Term Ice-Covered Freshwater Lakes in the Subarctic Region of Yakutia, Russia

  • Microbiology of Aquatic Systems
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Abstract

Although under-ice microbial communities are subject to a cold environment, low concentrations of nutrients, and a lack of light, they nevertheless take an active part in biogeochemical cycles. However, we still lack an understanding of how high their diversity is and how these communities are distributed during the long-term ice-cover period. Here, we assessed for the first time the composition and distribution of microbial communities during the ice-cover period in two subarctic lakes (Labynkyr and Vorota) located in the area of the lowest temperature in the Northern Hemisphere. The diversity distribution and abundance of main bacterial taxa as well as the composition of microalgae varied by time and habitat. The 16S rRNA gene sequencing method revealed, in general, a high diversity of bacterial communities where Proteobacteria (~ 45%) and Actinobacteria (~ 21%) prevailed. There were significant differences between the communities of the lakes: Chthoniobacteraceae, Moraxellaceae, and Pirellulaceae were abundant in Lake Labynkyr, while Cyanobiaceae, Oligoflexales, Ilumatobacteraceae, and Methylacidiphilaceae were more abundant in Lake Vorota. The most abundant families were evenly distributed in April, May, and June their contribution was different in different habitats. In April, Moraxellaceae and Ilumatobacteraceae were the most abundant in the water column, while Sphingomonadaceae was abundant both in water column and on the ice bottom. In May, the abundance of Comamonadaceae increased and reached the maximum in June, while Cyanobiaceae, Oxalobacteraceae, and Pirellulaceae followed. We found a correlation of the structure of bacterial communities with snow thickness, pH, Nmin concentration, and conductivity. We isolated psychrophilic heterotrophic bacteria both from dominating and minor taxa of the communities studied. This allowed for specifying their ecological function in the under-ice communities. These findings will advance our knowledge of the under-ice microbial life.

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References

  1. D’Amico S, Collins T, Marx J-C, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389. https://doi.org/10.1038/sj.embor.7400662

    Article  CAS  Google Scholar 

  2. De Maayer P, Anderson D, Cary C, Cowan DA (2014) Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep 15:508–517. https://doi.org/10.1002/embr.201338170

    Article  CAS  Google Scholar 

  3. Rodrigues DF, Tiedje JM (2008) Coping with our cold planet. Appl Environ Microbiol 74:1677–1686. https://doi.org/10.1128/AEM.02000-07

    Article  CAS  Google Scholar 

  4. Casanueva A, Tuffin M, Cary C, Cowan DA (2010) Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol 18:374–381. https://doi.org/10.1016/j.tim.2010.05.002

    Article  CAS  Google Scholar 

  5. Margesin R, Schinner F, Marx JC, Gerday C (2008) Psychrophiles, from Biodiversity to Biotechnology. Springer, Berlin

    Book  Google Scholar 

  6. Verpoorter C, Kutser T, Seekell DA, Tranvik LJ (2014) A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett 41:6396–6402. https://doi.org/10.1002/2014GL060641

    Article  Google Scholar 

  7. Hampton SE, Galloway AWE, Powers SM et al (2017) Ecology under lake ice. Ecol Lett 20:98–101. https://doi.org/10.1111/ele.12699

    Article  Google Scholar 

  8. Walsh SE, Vavrus SE, Foley JA, Fisher VA, Wynne RH, Lenters JD (1998) Global patterns of lake ice phenology and climate: model simulations and observations. J Geophys Res 103:28825–28837. https://doi.org/10.1029/98JD02275

    Article  Google Scholar 

  9. Salonen K, Leppa M, Viljanen RM, Gulati RD (2009) Perspectives in winter limnology: closing the annual cycle of freezing lakes. Aquat Ecol 43:609–616. https://doi.org/10.1007/s10452-009-9278-z

    Article  Google Scholar 

  10. Weyhenmeyer GAD, Livingstone M, Meili M, Jensen O, Benson B, Magnuso JJ (2011) Large geographical differences in the sensitivity of ice-covered lakes and rivers in the Northern Hemisphere to temperature changes. Glob Change Biol 17:268–275. https://doi.org/10.1111/j.1365-2486.2010.02249.x

    Article  Google Scholar 

  11. Bertilsson S, Burgin A, Carey CC, Fey SB, Grossart HP, Grubisic LM, Jones ID, Kirillin G, Lennon JT, Shade A, Smyth RL (2013) The under-ice microbiome of seasonally frozen lakes. Limnol Oceanogr 58:1998–2012. https://doi.org/10.4319/lo.2013.58.6.1998

    Article  Google Scholar 

  12. Powers SM, Hampton SE (2016) Winter limnology as a new frontier. Limnol Oceanogr Bull 25:103–108

    Article  Google Scholar 

  13. Wilhelm SW, LeCleir GR, Bullerjahn GS, McKay RM, Saxton MA, Twiss MR, Bourbonniere RA (2014) Seasonal changes in microbial community structure and activity imply winter production is linked to summer hypoxia in a large lake. FEMS Microbiol Ecol 87:475–485. https://doi.org/10.1111/1574-6941.12238

    Article  CAS  Google Scholar 

  14. Ricao Canelhas M, Denfeld BA, Weyhenmeyer GA, Bastviken D, Bertilsson S (2016) Methane oxidation at the water - ice interface of an ice-covered lake. Limnol Oceanogr 61:S79–S90. https://doi.org/10.1002/lno.10288

    Article  Google Scholar 

  15. Sommer U, Gliwicz ZM, Lampert W, Duncan A (1986) The PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hyrobiol 106:433–471

    Google Scholar 

  16. Bruesewitz DA, Carey CC, Richardson DC, Weathers KC (2015) Under-ice thermal stratification dynamics of a large, deep lake revealed by high-frequency data. Limnol Oceanogr 60:347–359. https://doi.org/10.1002/lno.10014

    Article  Google Scholar 

  17. Pernthaler J, Glöckner FO, Unterholzner S, Alfreider A, Psenner R, Amann R (1998) Seasonal community and population dynamics of pelagic bacteria and archaea in a high mountain lake. Appl Environ Microbiol 64:4299–4306. https://doi.org/10.1128/AEM.64.11.4299-4306.1998

    Article  CAS  Google Scholar 

  18. Beall BFN, Twiss MR, Smith DE, Oyserman BO, Rozmarynowycz MJ, Binding CE, Bourbonniere RA, Bullerjahn GS, Palmer ME, Reavie ED, Waters MK, Woityra WC, McKay RML (2016) Ice cover extent drives phytoplankton and bacterial community structure in a large north-temperate lake: implications for a warming climate. Environ Microbiol 18:1704–1719. https://doi.org/10.1111/1462-2920.12819

    Article  CAS  Google Scholar 

  19. Rogozin DY, Zykov VV, Chernetsky MY, Degermendzhy AG, Gulati RD (2009) Effect of winter conditions on distributions of anoxic phototrophic bacteria in two meromictic lakes in Siberia, Russia. Aquat Ecol 43:661–672. https://doi.org/10.1007/s10452-009-9270-7

    Article  CAS  Google Scholar 

  20. Villaescusa JA, Casamayor EO, Rochera C, Vela Zquez D, Chicote A, Quesada A, Camacho A (2010) A close link between bacterial community composition and environmental heterogeneity in maritime Antarctic lakes. Int Microbiol 13:67–77. https://doi.org/10.2436/20.1501.01.112

    Article  CAS  Google Scholar 

  21. Kirillin G, Leppäranta M, Terzhevik A, Granin N, Bernhardt J, Engelhardt C, Efremova T, Golosov S, Palshin N, Sherstyankin P, Zdorovennova G, Zdorovennov R (2012) Physics of seasonally ice-covered lakes: a review. Aquat Sci 74:659–682. https://doi.org/10.1007/s00027-012-0279-y

    Article  Google Scholar 

  22. Bižić-Ionescu M, Amann R, Grossart H-P (2014) Massive regime shifts and high activity of heterotrophic bacteria in an ice-covered lake. PLoS ONE 9(11):e113611. https://doi.org/10.1371/journal.pone.0113611

    Article  CAS  Google Scholar 

  23. Bashenkhaeva MV, Zakharova YR, Petrova DP, Khanaev IV, Galachyants YP, Likhoshway YV (2015) Sub-ice microalgal and bacterial communities in freshwater Lake Baikal, Russia. Microb Ecol 70:751–765. https://doi.org/10.1007/s00248-015-0619-2

    Article  Google Scholar 

  24. Bashenkhaeva MV, Zakharova YuR (2017) Cultivated bacteria from the sub-ice algaebacterial communities of Lake Baikal. Acta Biol Sibirica 3:76–85. https://doi.org/10.14258/abs.v3i3.3619

    Article  Google Scholar 

  25. Bashenkhaeva MV, Zakharova YuR, Galachyants YuP, Khanaev IV, YeV L (2017) Bacterial communities during the period of massive under-ice dinoflagellate development in Lake Baikal. Microbiol 86:524–532. https://doi.org/10.1134/S0026261717040038

    Article  CAS  Google Scholar 

  26. Bashenkhaeva MV, Galachyants YP, Khanaev IV, Sakirko MV, Petrova DP, YeV L, Zakharova YuR (2020) Comparative analysis of free-living and particle-associated bacterial communities of Lake Baikal during the ice-covered period. J Great Lakes Res 46:508–518. https://doi.org/10.1016/j.jglr.2020.03.015

    Article  Google Scholar 

  27. Cabello-Yeves PJ, Zemskaya TI, Rosselli R, Coutinho FH, Zakharenko AS, Blinov VV, Rodriguez-Valera F (2018) Genomes of novel microbial lineages assembled from the sub-ice waters of Lake Baikal. Appl Environ Microbiol 84:e02132-e2217. https://doi.org/10.1128/AEM.02132-17.e02132-17

    Article  Google Scholar 

  28. Butler TM, Wilhelm A-C, Dwyer AC, Webb PN, Baldwin AL, Techtmann SM (2019) Microbial community dynamics during lake ice freezing. Sci Rep 9:6231. https://doi.org/10.1038/s41598-019-42609-9

    Article  CAS  Google Scholar 

  29. Tran P, Ramachandran A, Khawasik O, Beisner BE, Rautio M, Huot Y, Walsh DA (2018) Microbial life under ice: metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice-covered lakes. Environ Microbiol 20:2568–2584. https://doi.org/10.1111/1462-2920.14283

    Article  CAS  Google Scholar 

  30. Somers DJ, Strock KE, Saros JE (2019) Environmental controls on microbial diversity in arctic lakes of West Greenland. Microb Ecol 80:6–72. https://doi.org/10.1007/s00248-019-01474-9

    Article  CAS  Google Scholar 

  31. Vigneron A, Lovejoy C, Cruaud P, Kalenitchenko D, Culley A, Vincent WF (2019) Contrasting winter versus summer microbial communities and metabolic functions in a permafrost Thaw lake. Front Microbiol 10:1656. https://doi.org/10.3389/fmicb.2019.01656

    Article  Google Scholar 

  32. Tomberg IV, Kopyrina LI, Bessudova AYu, Firsova AD, Bashenkhayeva MV, Zakharova YuR, Gorina EO (2017) Hydrochemistry and phytoplankton of the Lake Labynkyr and Lake Vorota (Sakha Republic). International conference “Lakes of Eurasia: problems and paths of their decision”, Conference Proceedings, Petrozavodsk, pp 426–432. (In Russian)

  33. Kopyrina L, Firsova A, Rodionova E, Zakharova Y, Bashenkhaeva M, Usoltseva M, Likhoshway Y (2020) The insight into diatom diversity, ecology, and biogeography of an extreme cold ultraoligotrophic Lake Labynkyr at the Pole of Cold in the northern hemisphere. Extremophiles 24:603–623. https://doi.org/10.1007/s00792-020-01181-1

    Article  Google Scholar 

  34. Usoltseva M, Kopyrina L, Titova L, Morozov A, Firsova A, Zakharova Y, Bashenkhaeva M, Maslennikova M, Likhoshway Y (2020) Finding of a putative Lake Baikal endemic, Lindavia minuta, in distant lakes near the Arctic pole in Yakutia (Russia). Diatom Res 35:141–153. https://doi.org/10.1080/0269249X.2020.1747551

    Article  Google Scholar 

  35. Zakharova YR, Bedoshvili YD, Petrova DP, Marchenkov AM, Volokitina NA, Bashenkhaeva MV, Kopyrina LI, Grachev MA, Likhoshway YV (2020) Morphological description and molecular phylogeny of two diatom clones from the genus Ulnaria (Kützing) Compère isolated from an ultraoligotrophic lake at the Pole of Cold in the Northern Hemisphere, Republic of Sakha (Yakutia), Russia. Cryptogam Algol 41:37–45. https://doi.org/10.5252/cryptogamie-algologie2020v41a6

    Article  Google Scholar 

  36. Kuzmin GV (1975) Techniques for studying biogeocenoses of inland water bodies. Nauka, Moscow (In Russian)

  37. Makarova IV, Pichkily LO (1970) To some problems on techniques of phytoplankton biomass estimation. Botanic J 55:1488–1494 (In Russian)

  38. Wetzel RG, Likens GE (2000) Composition and biomass of phytoplankton. In: Wetzel RG, Likens GE (eds) Limnological analyses. Springer Verlag, New York, pp 147–174

    Chapter  Google Scholar 

  39. Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. P Natl Acad Sci USA 82:6955–6959

    Article  CAS  Google Scholar 

  40. Denisova LY, Bel’kova NL, Tulokhonov II, Zaichikov EF (1999) Bacterial diversity at various depths in the southern part of Lake Baikal as revealed by 16S rDNA sequencing. Microbiol 68:475–483

    CAS  Google Scholar 

  41. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series 41:95–98

    CAS  Google Scholar 

  42. 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

    Article  CAS  Google Scholar 

  43. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S et al (2007) The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77. https://doi.org/10.1371/journal.pbio.0050077

    Article  CAS  Google Scholar 

  44. Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555. https://doi.org/10.1016/j.mimet.2003.08.009

    Article  CAS  Google Scholar 

  45. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  Google Scholar 

  46. Rognes T, Flouri T, Nichols B, Quince C, Mahe F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584doi:10.7717/peerj.2584

  47. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. https://doi.org/10.1128/AEM.01541-09

    Article  CAS  Google Scholar 

  48. Rohwer RR, Hamilton JJ, Newton RJ, McMahon KD (2018) TaxAss: leveraging a custom freshwater database achieves fine-scale taxonomic resolution. mSphere 3:e00327-18. https://doi.org/10.1128/mSphere.00327-18

    Article  CAS  Google Scholar 

  49. Oksanen J, Blanchet FG, Friendly M et al (2016) vegan: community ecology package. version 2.4–1. https://CRAN.R-project.org/package=vegan

  50. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  Google Scholar 

  51. Suzuki R, Terada Y, Shimodaira H (2019) pvclust: hierarchical clustering with p-values via multiscale bootstrap resampling. R package version 2.2-0. https://CRAN.R-project.org/package=pvclust

  52. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8

    Article  CAS  Google Scholar 

  53. Potapova NA, Nazyrova RI, Zabelina NM, Issaeva-Petrova LS, Korotkov VN, Otchagov DM (2006) Reference book of protected areas of the Russian Federation P II. ARRINP, Moscow

    Google Scholar 

  54. Bessudova AU, Tomberg IV, Firsova AD, Kopyrina LI, Likhoshway YV (2019) Silica-scaled chrysophytes in lakes Labynkyr and Vorota, of the Sakha (Yakutia) Republic, Russia. Nova Hedwigua 148:35–48. https://doi.org/10.1127/nova-suppl/2019/049

    Article  Google Scholar 

  55. Twiss MR, McKay RML, Bourbonniere RA, Bullerjahn GS, Carrick HJ, Smith REH, Winter JG, D’souza NA, Furey P, Lashaway AR, Saxton MA, Wilhelm SW (2012) Diatoms abound in ice-covered Lake Erie: an investigation of offshore winter limnology in Lake Erie over the period 2007 to 2010. J Great Lakes Res 38:18–30. https://doi.org/10.1016/j.jglr.2011.12.008

    Article  Google Scholar 

  56. D’souza NA, Kawarasaki Y, Ganyz JD et al (2013) Diatom assemblages promote ice formation in large lakes. ISME J 7:1632–1640

    Article  Google Scholar 

  57. Cruaud P, Vigneron A, Fradette M-S, Dorea CC, Culley AI, Rodriguez MJ, Charette SJ (2020) Annual bacterial community cycle in a seasonally ice-covered river reflects environmental and climatic conditions. Limnol Oceanogr 65:S21–S37. https://doi.org/10.1002/lno.1113

    Article  Google Scholar 

  58. Møller AK, Søborg DA, Abu Al-Soud W, Sørensen SJ, Kroer N (2013) Bacterial community structure in High-Arctic snow and freshwater as revealed by pyrosequencing of 16S rRNA genes and cultivation. Polar Res 32:17390. https://doi.org/10.3402/polar.v32i0.17390

    Article  Google Scholar 

  59. Papale M, Rizzo C, Villescusa JA, Rochera C, Camacho A, Michaud L, Lo Giudice A (2017) Prokaryotic assemblages in the maritime Antarctic Lake Limnopolar (Byers Peninsula, South Shetland Islands). Extremophiles 21:947–961. https://doi.org/10.1007/s00792-017-0955-x

    Article  CAS  Google Scholar 

  60. McKay RM, Prašil O, Pechar L, Lawrenz E, Rozmarynowycz MJ, Bullerjahn GS (2015) Freshwater ice as habitat: partitioning of phytoplankton and bacteria between ice and water in central European reservoirs. Environ Microbiol Rep 7:887–898. https://doi.org/10.1111/1758-2229.12322

    Article  CAS  Google Scholar 

  61. Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49. https://doi.org/10.1128/MMBR.00028-10

    Article  CAS  Google Scholar 

  62. Crump BC, Kling GW, Bahr M, Hobbie JE (2003) Bacterioplankton community shifts in an Arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69:2253–2268. https://doi.org/10.1128/AEM.69.4.2253-2268.2003

    Article  Google Scholar 

  63. Logares R, Lindstrӧm ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, Rengefors K, Tranvik L, Bertilsson S (2013) Ecology of microbial communities exposed to drastic long-term environmental change. ISME J 7:937–948. https://doi.org/10.1038/ismej.2012.168

    Article  CAS  Google Scholar 

  64. Mikhailov IS, Zakharova YR, Bukin YS, Galachyants YP, Petrova DP, Sakirko MV, Likhoshway YV (2019) Co-occurrence networks among bacteria and microbial eukaryotes of Lake Baikal during a spring phytoplankton bloom. Microb Ecol 77:96–109. https://doi.org/10.1007/s00248-018-1212-2

    Article  Google Scholar 

  65. Llorens-Marès T, Auguet JC, Casamayor EO (2012) Winter to spring changes in the slush bacterial community composition of a high-mountain lake (Lake Redon, Pyrenees). Environ Microbiol Rep 4:50–56. https://doi.org/10.1111/j.1758-2229.2011.00278.x

    Article  Google Scholar 

  66. Eiler A, Bertilsson S (2005) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6:1228–1243. https://doi.org/10.1111/j.1462-2920.2004.00657.x

    Article  Google Scholar 

  67. Pearce DA, van der Gast CJ, Lawley B, Ellis-Evans JC (2003) Bacterioplankton community diversity in a maritime Antarctic lake, determined by culture-dependent and culture-independent techniques. FEMS Microbiol Ecol 45:59–70. https://doi.org/10.1016/S0168-6496(03)00110-7

    Article  CAS  Google Scholar 

  68. Miteva V, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70:202–213. https://doi.org/10.1128/AEM.70.1.202-213.2004

    Article  CAS  Google Scholar 

  69. Michaud L, Caruso C, Mangano S, Interdonato F, Bruni V, Lo Giudice A (2012) Predominance of Flavobacterium, Pseudomonas, and Polaromonas within the prokaryotic community of freshwater shallow lakes in the northern Victoria Land, East Antarctica. FEMS Microbiol Ecol 82:391–404. https://doi.org/10.1111/j.1574-6941.2012.01394.x

    Article  CAS  Google Scholar 

  70. Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361. https://doi.org/10.1016/j.resmic.2010.12.004

    Article  Google Scholar 

  71. Abraham WP, Raghunandanan S, Gopinath V, Suryaletha K, Thomas S (2020) Deciphering the cold adaptive mechanisms in Pseudomonas psychrophila MTCC12324 Isolated from the Arctic at 79°N. Curr Microbiol 77:2345–2355. https://doi.org/10.1007/s00284-020-02006-2

    Article  CAS  Google Scholar 

  72. Bull AT (2011) Actinobacteria of the extremobiosphere. In: Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO (eds) Extremophiles handbook. Springer, Japan, pp 1203–1240

    Chapter  Google Scholar 

  73. Hansen AA, Herbert RA, Mikkelsen K, Jensen LL, Kristoffersen T, Tiedje JM, Lomstein BA, Finster KW (2007) Viability, diversity and composition of the bacterial community in a high Arctic permafrost soil from Spitsbergen, Northern Norway. Environ Microbiol 9:2870–2884. https://doi.org/10.1111/j.1462-2920.2007.01403.x

    Article  CAS  Google Scholar 

  74. Miteva V, Teacher C, Sowers T, Brenchley J (2009) Comparison of the microbial diversity at different depths of the GISP2 Greenland ice core in relationship to deposition climates. Environ Microbiol 11:640–656. https://doi.org/10.1111/j.1462-2920.2008.01835.x

    Article  CAS  Google Scholar 

  75. Vishnivetskaya TA, Petrova MA, Urbance J, Ponder M, Moyer CL, Gilichinsky DA, Tiedje JM (2006) Bacterial community in ancient Siberian permafrost as characterized by culture and culture-independent methods. Astrobiology 6:400–414. https://doi.org/10.1089/ast.2006.6.400

    Article  CAS  Google Scholar 

  76. Steven B, Pollard WH, Greer CW, Whyte LG (2008) Microbial diversity and activity through a permafrost/ ground ice core profile from the Canadian high Arctic. Environ Microbiol 10:3388–3403. https://doi.org/10.1111/j.1462-2920.2008.01746.x

    Article  CAS  Google Scholar 

  77. Bottos EM, Vincent WF, Greer CW, Whyte LG (2008) Prokaryotic diversity of arctic ice shelf microbial mats. Environ Microbiol 10:950–966. https://doi.org/10.1111/j.1462-2920.2007.01516.x

    Article  CAS  Google Scholar 

  78. Durán N, Justo GZ, Ferreira CV, Melo PS, Cordi L, Martins D (2007) Violacein: properties and biological activities. Biotechnol Appl Biochem 48:127–133. https://doi.org/10.1042/BA20070115

    Article  CAS  Google Scholar 

  79. Baricz A, Teban A, Chiriac CM, Szekeres E, Farkas A, Nica M, Dascălu A, Oprișan C, Lavin P, Coman C (2018) Investigating the potential use of an Antarctic variant of Janthinobacterium lividum for tackling antimicrobial resistance in a One Health approach. Sci Rep 8:15272. https://doi.org/10.1038/s41598-018-33691-6

    Article  CAS  Google Scholar 

  80. Van Trappen S, Mergaert J, Van Eygen S, Dawyndt P, Cnockaert MC, Swings J (2002) Diversity of 746 heterotrophic bacteria isolated from microbial mats from ten Antarctic lakes. Syst Appl Microbiol 25:603–610. https://doi.org/10.1078/07232020260517742

    Article  Google Scholar 

  81. Peeters K, Hodgson DA, Convey P, Willems A (2011) Culturable diversity of heterotrophic bacteria in Forlidas Pond (Pensacola Mountains) and Lundstrom Lake (Shackleton Range), Antarctica. Microbiol Ecol 62:399–413

    Article  Google Scholar 

  82. Miteva VI, Brenchley JE (2005) Detection and isolation of ultrasmall microorganisms from a 120,000-year-old Greenland glacier ice core. Appl Environ Microbiol 71:7806–7818. https://doi.org/10.1128/AEM.71.12.7806-7818.2005

    Article  CAS  Google Scholar 

  83. Amato P, Hennebelle R, Magan O, Sancelm M, Delort A-M, Barbant C, Boutron C, Ferrari C (2007) Bacterial characterization of the snow cover at Spitzberg, Svalbard. FEMS Microbiol Ecol 59:255–264. https://doi.org/10.1111/j.1574-6941.2006.00198.x

    Article  CAS  Google Scholar 

  84. Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2001) Isolation of bacteria and 16S rDNAs from lake Vostok accretion ice. Environ Microbiol 3:570–577. https://doi.org/10.1046/j.1462-2920.2001.00226.x

    Article  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge I.E. Zhullyarov and A.A. Dolzhenkov for organizing the expedition and technical support, and the divers A.S. Gubin, M.V. Astakhov, S.V. Bulochkin, and V.I. Chernykh for their assistance during the field studies.

Funding

The work was supported by the State Assignments of the Institute for Biological Problems of Cryolithozone, (No. 0297-2021-0023, 21-121012190038-0; expeditions) and of the Limnological Institute (No. 0279-2021-0008, 121032300186-9; analysis) of the Siberian Branch of the Russian Academy of Sciences. The microscopy studies were done in the Electron Microscopy Center of the Shared Research Facilities “Ultramicroanalysis” of Limnological Institute (https ://www.lin.irk.ru/copp/).

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  1. Limnological Institute, Siberian Branch of the Russian Academy of Sciences, 3 Ulan-Batorskaya Street, Irkutsk, 664033, Russia

    Yulia Zakharova, Maria Bashenkhaeva, Yuri Galachyants, Darya Petrova, Irina Tomberg, Artyom Marchenkov & Yelena Likhoshway

  2. Institute for Biological Problems of Cryolithozone, Siberian Branch of the Russian Academy of Sciences, 41 Lenin Ave, Yakutsk, 677980, Russia

    Liubov Kopyrina

Authors
  1. Yulia Zakharova
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  2. Maria Bashenkhaeva
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  3. Yuri Galachyants
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  4. Darya Petrova
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  5. Irina Tomberg
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  6. Artyom Marchenkov
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  7. Liubov Kopyrina
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  8. Yelena Likhoshway
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Contributions

Ye.L. and L.K. designed the study. Yu.Z., M.B., and L.K. were involved in the field work. M.B. and Yu.Z. identified species and cultivated of bacteria. D.P. and A.M. conducted molecular experiments. I.T. conducted chemical analyses. Yu.G. and M.B. analyzed the data and produced figures. Yu.Z. wrote the manuscript. Yu.Z., Yu.G., M.B., and Ye.L. contributed to revisions.

Corresponding author

Correspondence to Maria Bashenkhaeva.

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The authors declare no competing interests.

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Zakharova, Y., Bashenkhaeva, M., Galachyants, Y. et al. Variability of Microbial Communities in Two Long-Term Ice-Covered Freshwater Lakes in the Subarctic Region of Yakutia, Russia. Microb Ecol 84, 958–973 (2022). https://doi.org/10.1007/s00248-021-01912-7

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  • DOI: https://doi.org/10.1007/s00248-021-01912-7

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