Cite this paper:
Evgeniya MATYUGINA, Natalia BELKOVA, Svetlana BORZENKO, Pavel LUKYANOV, Marsel KABILOV, Olga BATURINA, Alexandra MARTYNOVA-VAN KLEY, Armen NALIAN, Aleksei PTITSYN. Structure and diversity dynamics of microbial communities at day and night: investigation of meromictic Lake Doroninskoe, Transbaikalia, Russia[J]. HaiyangYuHuZhao, 2018, 36(6): 1978-1992

Structure and diversity dynamics of microbial communities at day and night: investigation of meromictic Lake Doroninskoe, Transbaikalia, Russia

Evgeniya MATYUGINA1, Natalia BELKOVA2, Svetlana BORZENKO1, Pavel LUKYANOV1, Marsel KABILOV3, Olga BATURINA3, Alexandra MARTYNOVA-VAN KLEY4, Armen NALIAN4, Aleksei PTITSYN1
1 Institute of Natural Resources, Ecology and Cryology SB RAS, Chita, Russia;
2 Limnological Institute SB RAS, Irkutsk, Russia;
3 Institute of Chemical Biology and Fundamental Medicine, Novosibirsk, Russia;
4 Stephen F. Austin State University, TX, USA
Extreme environmental conditions are key factors in the formation of the structure and diversity of microbial communities. In meromictic ecosystems, extreme conditions and a stable stratification of physical, chemical and biological parameters lead to diversity and heterogeneity of microenvironments. Lake Doroninskoe is located in an extreme geographical area and differs from other known meromictic reservoirs of the world by a low level of illumination in the chemocline and a rare type of alkaline water in sedimentary rocks formed by evaporative concentration. To understand the key factors that shape the composition and structure of the microbial community, the macro- and micro-variations in space and time are of great importance. We investigated the short-term dynamics of the structure and diversity of microbial communities of the meromictic soda lake, Lake Doroninskoe, at day and night using highthroughput sequencing and bioinformatics. Metagenomic analysis of 16S rRNA gene amplicons showed that the microbial communities had a high taxonomic diversity both at day and night. Sixteen bacterial and three archaeal phyla were identified. Proteobacteria were dominant and comprised 75% during the day, increasing to 90% at night. Metabolically stable denitrifying bacteria that were able to use a variety of alternative electron acceptors and electron donors were prevalent in Lake Doroninskoe. They belonged to the families Enterobacteriaceae (class Gammaproteobacteria) and Alcaligenaceae (class Betaproteobacteria). Statistically significant differences between day and night microbial communities were found. During the day, the microbial community was the most diverse. We discuss the peculiarities of the underexplored shortterm dynamics of the structure and diversity of the microbial communities of the meromictic soda Lake Doroninskoe, and propose topics for prospective studies.
Key words:    bacterial diversity|day-night dynamics|meromixis|Lake Doroninskoe|high-throughput amplicon sequencing   
Received: 2018-01-27   Revised:
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Articles by Evgeniya MATYUGINA
Articles by Natalia BELKOVA
Articles by Svetlana BORZENKO
Articles by Pavel LUKYANOV
Articles by Marsel KABILOV
Articles by Olga BATURINA
Articles by Alexandra MARTYNOVA-VAN KLEY
Articles by Armen NALIAN
Articles by Aleksei PTITSYN
Andrade K, Logemann J, Heidelberg K B, Emerson J B, Comolli L R, Hug L A, Probst A J, Keillar A, Thomas B C, Miller C S, Allen E E, Moreau J W, Brocks J J, Banfield J F. 2015. Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem. ISME Journal, 9(12):2 697-2 711.
Andrei A Ş, Robeson Ⅱ M S, Baricz A, Coman C, Muntean V, Ionescu A, Etiope G, Alexe M, Sicora C I, Podar M, Banciu H L. 2015. Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes. ISME Journal, 9(12):2 642-2 656.
Baatar B, Chiang P W, Rogozin D Y, Wu Y T, Tseng C H, Yang C Y, Chiu H H, Oyuntsetseg B, Degermendzhy A G, Tang S L. 2016. Bacterial communities of three saline meromictic lakes in Central Asia. PLoS One, 11(3):e0150847.
Borzenko S V, Zamana L V, Buryukhaev S P. 2014. The isotopic composition of dissolved carbonates as a reflection of abiogenic and biogenic processes in the water column of the Lake Doroninskoe. Razvitie zhizni v protsesse abioticheskikh izmenenij na Zamle, 3:319-323.(in Russian).
Borzenko S V, Zamana L V, Noskova E V. 2015. Meromixis of the Lake Doroninskoye (Eastern Transbaikalia). Geological and Mineralogical sciences, 1:420-425. (in Russian).
Borzenko S V, Zamana L V. 2011. Reduced forms of sulfur in the brine of saline-soda Lake Doroninskoe, eastern Transbaikal region. Geochemistry International, 49(3):253-261. (in Russian)
Bosshard P P, Santini Y, Grüter D, Stettler R, Bachofen R. 2000. Bacterial diversity and community composition in the chemocline of the meromictic alpine Lake Cadagno as revealed by 16S rDNA analysis. FEMS Microbiology Ecology, 31(2):173-182.
Comeau A M, Harding T, Galand P E, Vincent W F, Lovejoy C. 2012. Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Scientific Reports, 2:604.
Dimitriu P A, Pinkart H C, Peyton B M, Mormile M R. 2008.Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in Washington State. Applied and Environmental Microbiology, 74(15):4 877-4 888.
Dvornyk V, Vinogradova O, Nevo E. 2003. Origin and evolution of circadian clock genes in prokaryotes.Proceedings of the National Academy of Sciences of the United States of America, 100(5):2 495-2 500.
Edgar R C. 2013. UPARSE:highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10):996-998.
Fadrosh D W, Ma B, Gajer P, Sengamalay N, Ott S, Brotman R M, Ravel J. 2014. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome, 2:6.
Falagán C, Sánchez-España J, Johnson D B. 2014. New insights into the biogeochemistry of extremely acidic environments revealed by a combined cultivation-based and culture-independent study of two stratified pit lakes.FEMS Microbiology Ecology, 87(1):231-243.
Frigaard N U, Dahl C. 2008. Sulfur metabolism in phototrophic sulfur bacteria. Advances in Microbial Physiology, 54:103-200.
Garcia S L, Salka I, Grossart H P, Warnecke F. 2013. Depthdiscrete profiles of bacterial communities reveal pronounced spatio-temporal dynamics related to lake stratification. Environmental Microbiology Reports, 5(4):549-555.
Garcia-Gil L J, Casamitjana X, Abella C A. 1996. Comparative study of two meromictic basins of Lake Banyoles (Spain)with sulphur phototrophic bacteria. Hydrobiologia, 319(3):203-211.
Gifford S M, Sharma S, Moran M A. 2014. Linking activity and function to ecosystem dynamics in a coastal bacterioplankton community. Frontiers in Microbiology, 5:185.
Gilbert J A, Field D, Swift P, Thomas S, Cummings D, Temperton B, Weynberg K, Huse S, Hughes M, Joint I, Somerfield P J, Mühling M. 2010. The taxonomic and functional diversity of microbes at a temperate coastal site:a ‘Multi-Omic’ study of seasonal and diel temporal variation. PLoS One, 5(11):e15545.
Gorlenko V M, Buryukhaev S P, Matyugina E B, Borzenko S V, Namsaraev Z B, Bryantseva I A, Boldareva E N, Sorokin D Y, Namsaraev B B. 2010. Microbial communities of the stratified soda Lake Doroninskoe(Transbaikal region). Microbiology, 79(3):390-401.
Gregersen L H, Habicht K S, Peduzzi S, Tonolla M, Canfield D E, Miller M, Cox R P, Frigaard N U. 2009. Dominance of a clonal green sulfur bacterial population in a stratified lake. FEMS Microbiology Ecology, 70(1):30-41.
Gulati R D, Zadereev E S, Degermendzhi A G. 2017. Ecology of Meromictic Lakes. Springer, Cham. 405p.
Gunnigle E, Frossard A, Ramond J B, Guerrero L, Seely M, Cowan D A. 2017. Diel-scale temporal dynamics recorded for bacterial groups in Namib Desert soil. Scientific Reports, 7:40 189.
Habicht K S, Miller M, Cox R P, Frigaard N U, Tonolla M, Peduzzi S, Falkenby L G, Andersen J S. 2011. Comparative proteomics and activity of a green sulfur bacterium through the water column of Lake Cadagno, Switzerland.Environmental Microbiology, 13(1):203-215.
Hamilton T L, Bovee R J, Sattin S R, Mohr W, Gilhooly Ⅲ W P, Lyons T W, Pearson A, Macalady J L. 2016. Carbon and sulfur cycling below the chemocline in a meromictic lake and the identification of a novel taxonomic lineage in the FCB Superphylum, Candidatus Aegiribacteria. Frontiers in Microbiology, 7:598.
Hashsham S A, Fernandez A S, Dollhopf S L, Dazzo F B, Hickey R F, Tiedje J M, Criddle C S. 2000. Parallel processing of substrate correlates with greater functional stability in methanogenic bioreactor communities perturbed by glucose. Applied and Environmental Microbiology, 66(9):4 050-4 057.
Hewson I, Poretsky R S, Tripp H J, Montoya J P, Zehr J P. 2010. Spatial patterns and light-driven variation of microbial population gene expression in surface waters of the oligotrophic open ocean. Environmental Microbiology, 12(27):1 940-1 956.
Humayoun S B, Bano N, Hollibaugh J T. 2003. Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Applied and Environmental Microbiology, 69(2):1 030-1 042.
Hut R A, Beersma D G M. 2011. Evolution of time-keeping mechanisms:early emergence and adaptation to photoperiod. Philosophical Transactions of the Royal Society B:Biological Sciences, 366(1574):2 141-2 154.
Imhoff J F. 2016. New dimensions in microbial ecology-functional genes in studies to unravel the biodiversity and role of functional microbial groups in the environment.Microorganisms, 4(2):19.
Johnson D B, Hallberg K B. 2009. Carbon, iron and sulfur metabolism in acidophilic micro-organisms. Advances in Microbial Physiology, 54:201-255.
Koizumi Y, Kojima H, Fukui M. 2004a. Dominant microbial composition and its vertical distribution in saline meromictic Lake Kaiike (Japan) as revealed by quantitative oligonucleotide probe membrane hybridization. Applied and Environmental Microbiology, 70(8):4 930-4 940.
Koizumi Y, Kojima H, Oguri K, Kitazato H, Fukui M. 2004b.Vertical and temporal shifts in microbial communities in the water column and sediment of saline meromictic Lake Kaiike (Japan), as determined by a 16S rDNA-based analysis, and related to physicochemical gradients.Environmental Microbiology, 6(6):622-637.
Lanzén A, Simachew A, Gessesse A, Chmolowska D, Jonassen I, Øvreås L. 2013. Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian Soda Lakes. PLoS One, 8(8):e72577.
Lauro F M, De Maere M Z, Yau S, Brown M V, Ng C, Wilkins D, Raftery M J, Gibson J A, Andrews-Pfannkoch C, Lewis M, Hoffman J M, Thomas T, Cavicchioli R. 2011. An integrative study of a meromictic lake ecosystem in Antarctica. ISME Journal, 5(5):879-895.
Leboulanger C, Agogué H, Bernard C, Bouvy M, Carré C, Cellamare M, Duval C, Fouilland E, Got P, Intertaglia L, Lavergne C, Le Floc'h E, Roques C, Sarazin G. 2017.Microbial diversity and cyanobacterial production in Dziani Dzaha crater Lake, a unique tropical thalassohaline environment. PLoS One, 12(1):e0168879.
Lehours A C, Bardot C, Thenot A, Debroas D, Fonty G. 2005.Anaerobic microbial communities in Lake Pavin, a unique meromictic Lake in France. Applied and Environmental Microbiology, 71(11):7 389-7 400.
Lehours A C, Evans P, Bardot C, Joblin K, Gérard F. 2007.Phylogenetic diversity of archaea and bacteria in the anoxic zone of a meromictic lake (Lake Pavin, France).Applied and Environmental Microbiology, 73(6):2 016-2 019.
Lindström E S, Langenheder S. 2012. Local and regional factors influencing bacterial community assembly.Environmental Microbiology Reports, 4(1):1-9.
Lozupone C A, Knight R. 2007. Global patterns in bacterial diversity. Proceedings of the National Academy of Sciences of the United States of America, 104(27):11 436-11 440.
Matyugina E B, Borzenko S V, Matafonov P V, Belkova N L. 2014. A laboratory experiment for meromixis in an integrated sample of soda Lake Doroninskoye(Transbaikalia). Current Research in Microbiology and Biotechnology, 2(3):398-401.
Matyugina E, Belkova N. 2015. Distribution and diversity of microbial communities in meromictic soda Lake Doroninskoe (Transbaikalia, Russia) during winter.Chinese Journal of Oceanology and Limnology, 33(6):1 378-1 390.
Meuser J E, Baxter B K, Spear J R, Peters J W, Posewitz M C, Boyd E S. 2013. Contrasting patterns of community assembly in the stratified water column of Great Salt Lake, Utah. Microbial Ecology, 66(2):268-280.
Oksanen J, Blanchet F G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P R, O'Hara R B, Simpson G L, Solymos P, Stevens M H H, Szoecs E, Wagner H. 2018.Vegan:Community Ecology Package.
Ottesen E A, Young C R, Gifford S M, Eppley J M, Marin Ⅲ R, Schuster S C, Scholin C A, DeLong E F. 2014. Ocean microbes. Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science, 345(6193):207-212.
Overmann J, Beatty J T, Hall K J, Pfennig N, Northcote T G. 1991. Characterization of a dense, purple sulfur bacterial layer in a meromictic salt lake. Limnology and Oceanography, 36(5):846-859.
Poretsky R S, Hewson I, Sun S L, Allen A E, Zehr J P, Moran M A. 2009. Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific subtropical gyre. Environmental Microbiology, 11(6):1 358-1 375.
R Development Core Team. 2016. R:a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Robertson C E, Harris J K, Wagner B D, Granger D, Browne K, Tatem B, Feazel L M, Park K, Pace N R, Frank D N. 2013. Explicet:Graphical user interface software for metadata-driven management, analysis and visualization of microbiome data. Bioinformatics, 29(23):3 100-3 101.
Shilova I N, Robidart J C, DeLong E F, Zehr J P. 2016. Genetic diversity affects the daily transcriptional oscillations of marine microbial populations. PLoS One, 11(1):e0146706.
Silveira C B, Gregoracci G B, Coutinho F H, Silva G G Z, Haggerty J M, de Oliveira L S, Cabral A S, Rezende C E, Thompson C C, Francini-Filho R B, Edwards R A, Dinsdale E A, Thompson F L. 2017. Bacterial community associated with the reef coral Mussismilia braziliensis's momentum boundary layer over a diel cycle. Frontiers in Microbiology, 8:784.
Sorokin D Y, Foti M, Pinkart H C, Muyzer G. 2007. Sulfuroxidizing bacteria in Soap Lake (Washington State), a meromictic, haloalkaline lake with an unprecedented high sulfide content. Applied and Environmental Microbiology, 73(2):451-455.
Sorokin D Y, Gorlenko V M, Tourova T P, Tsapin A I, Nealson K H, Kuenen G J. 2002. Thioalkalimicrobium cyclicum sp. nov. and Thioalkalivibrio jannaschii sp. nov., novel species of haloalkaliphilic, obligately chemolithoautotrophic sulfur-oxidizing bacteria from hypersaline alkaline Mono Lake (California).International Journal of Systematic and Evolutionary Microbiology, 52(3):913-920.
Tagkopoulos I, Liu Y C, Tavazoie S. 2008. Predictive behavior within microbial genetic networks. Science, 320(5881):1 313-1 317.
Thorpe C L, Morris K, Boothman C, Lloyd J R. 2012. Alkaline Fe(Ⅲ) reduction by a novel alkali-tolerant Serratia sp.isolated from surface sediments close to Sellafield nuclear facility, UK. FEMS Microbiology Letters, 327(2):87-92.
Tonolla M, Peduzzi R, Hahn D. 2005. Long-term population dynamics of phototrophic sulfur bacteria in the chemocline of Lake Cadagno, Switzerland. Applied and Environmental Microbiology, 71(7):3 544-3 550.
Vila-Costa M, Sharma S, Moran M A, Casamayor E O. 2013.Diel gene expression profiles of a phosphorus limited mountain lake using metatranscriptomics. Environmental Microbiology, 15(4):1 190-1 203.
Volkov I I, Zhabina N N. 1990. Method of determination of reduced sulfur-compounds in the sea-water Okeanologiya, 30(5):778-782.
Wang J J, Yang D M, Zhang Y, Shen J, van der Gast C, Hahn M W, Wu Q L. 2011. Do patterns of bacterial diversity along salinity gradients differ from those observed for macroorganisms? PLoS One, 6(11):e27597.
Wang Q, Garrity G M, Tiedje J M, Cole J R. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16):5 261-5 267.
Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, de Vos P, Verstraete W, Boon N. 2009. Initial community evenness favours functionality under selective stress. Nature, 458(7238):623-626.
Zamana L V, Borzenko S V. 2007. Hydrogen sulfide and other reduced forms of sulfur in oxic waters of Lake Doroninskoe, Eastern Transbaikalia. Doklady Earth Sciences, 417(1):1 268-1 271.
Zerkle A L, Kamyshny A Jr, Kump L R, Farquhar J, Oduro H, Arthur M A. 2010. Sulfur cycling in a stratified euxinic lake with moderately high sulfate:constraints from quadruple S isotopes. Geochimica et Cosmochimica Acta, 74(17):4 953-4 970.
Zhang F, Vicente J, Hill R T. 2014. Temporal changes in the diazotrophic bacterial communities associated with Caribbean sponges Ircinia stroblina and Mycale laxissima.Frontiers in Microbiology, 5:561.
Zhong Z P, Liu Y, Miao L L, Wang F, Chu L M, Wang J L, Liu Z P. 2016. Prokaryotic community structure driven by salinity and ionic concentrations in Plateau Lakes of the Tibetan plateau. Applied and Environmental Microbiology, 82(6):1 846-1 858.