Microbial communities involved in the methane cycle in the near-bottom water layer and sediments of the meromictic subarctic Lake Svetloe
Although arctic and subarctic lakes are important sources of methane, the emission of which will increase due to the melting of permafrost, the processes related to the methane cycle in such environments are far from being comprehensively understood. Here we studied the microbial communities in the near-bottom water layer and sediments of the meromictic subarctic Lake Svetloe using high-throughput sequencing of the 16S rRNA and methyl coenzyme M reductase subunit A genes. Hydrogenotrophic methanogens of the order Methanomicrobiales were abundant, both in the water column and in sediments, while the share of acetoclastic Methanosaetaceae decreased with the depth of sediments. Members of the Methanomassiliicoccales order were absent in the water but abundant in the deep sediments. Archaea known to perform anaerobic oxidation of methane were not found. The bacterial component of the microbial community in the bottom water layer included oxygenic (Cyanobacteria) and anoxygenic (Chlorobi) phototrophs, aerobic Type I methanotrophs, methylotrophs, syntrophs, and various organotrophs. In deeper sediments the diversity of the microbial community decreased, and it became dominated by methanogenic archaea and the members of the Bathyarchaeota, Chloroflexi and Deltaproteobacteria. This study shows that the sediments of a subarctic meromictic lake contain a taxonomically and metabolically diverse community potentially capable of complete mineralization of organic matter.
KeywordsFreshwater lake Microbial diversity sediments Methanogenesis
The authors thank N. Kokryatskaya and A. Chupakov (Federal Research Centre for Integrated Studies of the Arctic) for their help in the sampling of primary material. This work was performed using the scientific equipment of the Core Research Facility “Bioengineering” and was partly supported by the Russian Science Foundation (Grant Number 16-14-10201). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Conflict of interest
The authors declare that they have no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Borrel G, Lehours AC, Crouzet O, Jézéquel D, Rockne K, Kulczak A, Duffaud E, Joblin K, Fonty G (2012) Stratification of Archaea in the deep sediments of a freshwater meromictic lake: vertical shift from methanogenic to uncultured archaeal lineages. PLoS ONE 7:e43346CrossRefPubMedPubMedCentralGoogle Scholar
- Borrel G, Adam PS, McKay LJ, Chen LX, Sierra-García IN, Sieber CMK, Letourneur Q, Ghozlane A, Andersen GL, Li WJ, Hallam SJ, Muyzer G, de Oliveira VM, Inskeep WP, Banfield JF, Gribaldo S (2019) Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nat Microbiol 4(4):603–613CrossRefPubMedGoogle Scholar
- Castelle CJ, Wrighton KC, Thomas BC, Hug LA, Brown CT, Wilkins MJ, Frischkorn KR, Tringe SG, Singh A, Markillie LM, Taylor RC, Williams KH, Banfield JF (2015) Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol 25(6):690–701CrossRefPubMedGoogle Scholar
- Concheri G, Stevanato P, Zaccone C, Shotyk W, D’Orazio V, Miano T, Piffanelli P, Rizzi V, Ferrandi C, Squartini A (2017) Rapid peat accumulation favours the occurrence of both fen and bog microbial communities within a Mediterranean, free-floating peat island. Sci Rep 7:8511CrossRefPubMedPubMedCentralGoogle Scholar
- Corinne BP, Najwa T, Hélène G, Corentin H, Didier D (2018) New insights into the pelagic microorganisms involved in the methane cycle in the meromictic Lake Pavin through metagenomics. FEMS Microbiol Ecol 95(3):fiy183Google Scholar
- Davis JP, Youssef NH, Elshahed MS (2009) Assessment of the diversity, abundance, and ecological distribution of members of candidate division SR1 reveals a high level of phylogenetic diversity but limited morphotypic diversity. Appl Environ Microbiol 75(12):4139–4148CrossRefPubMedPubMedCentralGoogle Scholar
- Ershova AA, Vorobyeva TYa, Moreva OYu, Chupakov AV, Zabelina SA, Neverova NV (2015) Hydrochemical and microbiological research of a nitrogen cycle in freshwater meromictic Lake Svetloe (the Arkhangelsk region). Reg Environ Issues 5:44–50 (in Russian) Google Scholar
- Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJCT, van Alen T, Luesken F, Wu MV, van de Pas-Schoonen KT, Op den Camp HJM, Janssen-Megens EM, Francoijs K-J, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548CrossRefPubMedGoogle Scholar
- Imhoff JF (2014) Biology of green sulfur bacteria. eLS. https://doi.org/10.1002/9780470015902.a0000458.pub2 CrossRefGoogle Scholar
- Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, Bergamaschi P, Bergmann D, Blake DR, Bruhwiler L, Cameron-Smith P, Castaldi S, Chevallier F, Feng L, Fraser A, Heimann M, Hodson EL, Houweling S, Josse B, Fraser PJ, Krummel PB, Lamarque J-F, Langenfelds RL, Quéré CL, Naik V, O’Doherty S, Palmer PI, Pison I, Plummer D, Poulter B, Prinn RG, Rigby M, Ringeval B, Santini M, Schmidt M, Shindell DT, Simpson IJ, Spahni R, Steele LP, Strode SA, Sudo K, Szopa S, van der Werf GR, Voulgarakis A, van Weele M, Weiss RF, Williams JE, Zeng G (2013) Three decades of global methane sources and sinks. Nat Geosci 6:813–823CrossRefGoogle Scholar
- Kuever J (2014) The family syntrophaceae. In: The prokaryotes. Springer, Berlin, pp 281–288Google Scholar
- Nobu MK, Dodsworth JA, Murugapiran SK, Rinke C, Gies EA, Webster G, Schwientek P, Kille P, Parkes RJ, Sass H, Jørgensen BB, Weightman AJ, Liu W-L, Hallam SJ, Tsiamis G, Woyke T, Hedlund BP (2016) Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics. ISME J 10(2):273–286CrossRefGoogle Scholar
- Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu W-T, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499(7459):431–437CrossRefGoogle Scholar
- Savvichev AS, Kokryatskaya NM, Zabelina SA, Rusanov II, Zakharova EE, Veslopolova EF, Lunina ON, Patutina EO, Bumazhkin BK, Gruzdev DS, Sigalevich PA, Pimenov NV, Kuznetsov BB, Gorlenko VM (2017) Microbial processes of the carbon and sulfur cycles in an ice-covered, iron-rich meromictic Lake Svetloe (Arkhangelsk region, Russia). Environ Microbiol 19(2):659–672CrossRefPubMedGoogle Scholar
- Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
- Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSJ, Chan PP, Gollabgir A, Hemp J, Hьgler M, Karr EA, Kцnneke M, Shin M, Lawton TJ, Lowe T, Martens-Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107(19):8818–8823CrossRefPubMedGoogle Scholar
- Wilson K (2003) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Wiley, New York, pp 2.4.1–2.4.5Google Scholar
- Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, Harada H, Kamagata Y (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evol Microbiol 56(6):1331–1340CrossRefGoogle Scholar