Skip to main content

Advertisement

SpringerLink
Log in

Spatiotemporal Changes in the Bacterial Community of the Meromictic Lake Uchum, Siberia

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Lake Uchum is a newly defined meromictic lake in Siberia with clear seasonal changes in its mixolimnion. This study characterized the temporal dynamics and vertical profile of bacterial communities in oxic and anoxic zones of the lake across all four seasons: October (autumn), March (winter), May (spring), and August (summer). Bacterial richness and diversity in the anoxic zone varied widely between time points. Proteobacteria was the dominant bacterial phylum throughout the oxic and anoxic zones across all four seasons. Alphaproteobacteria (Loktanella) and Gammaproteobacteria (Aliidiomarina) exhibited the highest abundance in the oxic and anoxic zone, respectively. Furthermore, there was a successional shift in sulfate-reducing bacteria (SRB) and sulfur-oxidizing bacteria in the anoxic zone across the seasons. The most dominant SRB, Desulfonatronovibrio sp., is likely one of the main producers of hydrogen sulfide (H2S) and typically accumulates the most H2S in winter. The representative anoxygenic phototrophic bacterial group in Lake Uchum was purple sulfur bacteria (PSB). PSB were dominant (60.76%) in summer, but only had 0.2–1.5% relative abundance from autumn to spring. Multivariate analysis revealed that the abundance of these SRB and PSB correlated to the concentration of H2S in Lake Uchum. Taken together, this study provides insights into the relationships between changes in bacterial community and environmental features in Lake Uchum.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Zadereev ES, Boehrer B, Gulati RD (2017) Introduction: meromictic lakes, their terminology and geographic distribution. Ecology of Meromictic lakes. Springer, pp. 1–11

  2. Alcocer J (2017) Mexican meromictic lakes: what we know so far. Ecology of Meromictic Lakes. Springer, pp. 353-375

  3. Lewis T, Francus P, Bradley RS (2007) Limnology, sedimentology, and hydrology of a jökulhlaup into a meromictic high arctic lake. Can J Earth Sci 44:791–806

    Article  Google Scholar 

  4. Inceoğlu Ö, Llirós M, García-Armisen T, Crowe SA, Michiels C, Darchambeau F, Descy J-P, Servais P (2015) Distribution of bacteria and archaea in meromictic tropical Lake Kivu (Africa). Aquat Microb Ecol 74:215–233

    Article  Google Scholar 

  5. Hall KJ, Northcote TG (2012) Meromictic lakes. Encyclopedia of Lakes and Reservoirs:519–524

  6. Wu Y-T, Yang C-Y, Chiang P-W, Tseng C-H, Chiu H-H, Saeed I, Baatar B, Rogozin DY, Halgamuge S, Degermendzhi A (2018) Comprehensive insights into composition, metabolic potentials, and interactions among archaeal, bacterial, and viral assemblages in meromictic lake Shunet in Siberia. Front Microbiol 9: 1763

  7. Lauro FM, DeMaere MZ, Yau S, Brown MV, Ng C, Wilkins D, Raftery MJ, Gibson JA, Andrews-Pfannkoch C, Lewis M (2011) An integrative study of a meromictic lake ecosystem in Antarctica. The ISME journal 5:879–895

    Article  CAS  PubMed  Google Scholar 

  8. Baatar B, Chiang P-W, Rogozin DY, Wu Y-T, Tseng C-H, Yang C-Y, Chiu H-H, Oyuntsetseg B, Degermendzhy AG, Tang S-L (2016) Bacterial communities of three saline meromictic lakes in Central Asia. PLoS One 11:e0150847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Gies EA, Konwar KM, Beatty JT, Hallam SJ (2014) Illuminating microbial dark matter in meromictic Sakinaw Lake. Appl Environ Microbiol 80:6807–6818

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Raffa C, Rizzo C, Strous M, De Domenico E, Sanfilippo M, Michaud L, Lo Giudice A (2019) Prokaryotic dynamics in the meromictic coastal lake Faro (Sicily, Italy). Diversity 11: 37

  11. Peura S, Eiler A, Bertilsson S, Nykänen H, Tiirola M, Jones RI (2012) Distinct and diverse anaerobic bacterial communities in boreal lakes dominated by candidate division OD1. The ISME journal 6:1640–1652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. İnceoğlu Ö, Llirós M, Crowe SA, García-Armisen T, Morana C, Darchambeau F, Borges AV, Descy J-P, Servais P (2015) Vertical distribution of functional potential and active microbial communities in meromictic Lake Kivu. Microb Ecol 70: 596–611

  13. Overmann J, Beatty JT, Hall KJ, Pfennig N, Northcote TG (1991) Characterization of a dense, purple sulfur bacterial layer in a meromictic salt lake. Limnol Oceanogr 36:846–859

    Article  CAS  Google Scholar 

  14. Frigaard N-U, Dahl C (2008) Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54:103–200

    Article  CAS  Google Scholar 

  15. Gregersen LH, Bryant DA, Frigaard N-U (2011) Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front Microbiol 2:116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Oikonomou A, Pachiadaki M, Stoeck T (2014) Protistan grazing in a meromictic freshwater lake with anoxic bottom water. FEMS Microbiol Ecol 87:691–703

    Article  CAS  PubMed  Google Scholar 

  17. Bush T, Diao M, Allen RJ, Sinnige R, Muyzer G, Huisman J (2017) Oxic-anoxic regime shifts mediated by feedbacks between biogeochemical processes and microbial community dynamics. Nat Commun 8:1–9

    Article  CAS  Google Scholar 

  18. Diao M, Huisman J, Muyzer G (2018) Spatio-temporal dynamics of sulfur bacteria during oxic--anoxic regime shifts in a seasonally stratified lake. Fems Microbiol Ecol 94: fiy040

  19. Boehrer B, von Rohden C, Schultze M (2017) Physical features of meromictic lakes: stratification and circulation. Ecology of Meromictic lakes. Springer, pp. 15-34

  20. Rogozin D, Zykov V, Ivanova E, Anufrieva T, Barkhatov Y, Khromechek E, Botvich I (2018) Meromixis and seasonal dynamics of vertical structure of Lake Uchum (South Siberia). Contemp Probl Ecol 11: 195–206

  21. Tonolla M, Peduzzi S, Hahn D, Peduzzi R (2003) Spatio-temporal distribution of phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno (Switzerland). FEMS Microbiol Ecol 43: 89–98

  22. Comeau AM, Harding T, Galand PE, Vincent WF, Lovejoy C (2012) Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Sci Rep 2:604

    Article  PubMed  PubMed Central  Google Scholar 

  23. Volkov I, Zhabina N (1990) Method of determination of reduced sulfur-compounds in the sea-water. Okeanologiya 30:778–782

    CAS  Google Scholar 

  24. Rogozin DY, Trusova MY, Khromechek E, Degermendzhy A (2010) Microbial community of the chemocline of the meromictic Lake Shunet (Khakassia, Russia) during summer stratification. Microbiology+ 79: 253-261

  25. Wilson K (2001) Preparation of genomic DNA from bacteria. Current protocols in molecular biology 56: 2.4. 1–2.4. 5

  26. Tandon K, Yang S-H, Wan M-T, Yang C-C, Baatar B, Chiu C-Y, Tsai J-W, Liu W-C, Tang S-L (2018) Bacterial community in water and air of two sub-alpine lakes in Taiwan. Microbes and environments: ME17148

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

    Article  CAS  PubMed  Google Scholar 

  28. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Glöckner FO, Yilmaz P, Quast C, Gerken J, Beccati A, Ciuprina A, Bruns G, Yarza P, Peplies J, Westram R (2017) 25 years of serving the community with ribosomal RNA gene reference databases and tools. J Biotechnol 261:169–176

    Article  PubMed  CAS  Google Scholar 

  30. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:W20–W25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

    Article  CAS  PubMed  Google Scholar 

  34. Kalyaanamoorthy S, Minh BQ, Wong TK, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Minh BQ, Nguyen MAT, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible Interactive analysis and graphics of microbiome census data. PLoS One 8: e61217

  38. Racine JS (2012) RStudio: a platform-independent IDE for R and Sweave. J Appl Econ 27:167–172

    Article  Google Scholar 

  39. Clarke K, Gorley R (2005) PRIMER: getting started with v6. PRIMER-E Ltd: Plymouth, UK

  40. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community ecology package 10:631–637

    Google Scholar 

  41. Dimitriu PA, Pinkart HC, Peyton BM, Mormile MR (2008) Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in Washington State. Appl Environ Microbiol 74:4877–4888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Northcote T, Halsey T (1969) Seasonal changes in the limnology of some meromictic lakes in southern British Columbia. J Fish Board Can 26: 1763–1787

  43. Parker R, Lawrence J, Hammer U (1983) A comparison of phototrophic bacteria in two adjacent saline meromictic lakes. Hydrobiologia 105:53–61

    Article  CAS  Google Scholar 

  44. Chiu H-H, Rogozin DY, Huang S-P, Degermendzhy AG, Shieh WY, Tang S-L (2014) Aliidiomarina shirensis sp. nov., a halophilic bacterium isolated from Shira Lake in Khakasia, southern Siberia, and a proposal to transfer Idiomarina maris to the genus Aliidiomarina. Int J Syst Evol Microbiol 64: 1334–1339

  45. Srinivas T, Kumar PA (2012) Aliidiomarina haloalkalitolerans sp. nov., a marine bacterium isolated from coastal surface seawater. Antonie Van Leeuwenhoek 101:761–768

    Article  CAS  PubMed  Google Scholar 

  46. Zhang R-C, Xu X-J, Chen C, Shao B, Zhou X, Yuan Y, Lee D-J, Ren N-Q (2019) Bioreactor performance and microbial community analysis of autotrophic denitrification under micro-aerobic condition. Sci Total Environ 647:914–922

    Article  CAS  PubMed  Google Scholar 

  47. Li J, Brown ET, Crowe SA, Katsev S (2018) Sediment geochemistry and contributions to carbon and nutrient cycling in a deep meromictic tropical lake: Lake Malawi (East Africa). J Great Lakes Res 44: 1221–1234

  48. Matyugina E, Belkova N, Borzenko S, Lukyanov P, Kabilov M, Baturina O, Martynova-Van Kley A, Nalian A, Ptitsyn A (2018) Structure and diversity dynamics of microbial communities at day and night: investigation of meromictic Lake Doroninskoe, Transbaikalia, Russia. J Oceanol Limnol 36: 1978–1992

  49. Andrei A-Ş, Robeson II MS, Baricz A, Coman C, Muntean V, Ionescu A, Etiope G, Alexe M, Sicora CI, Podar M (2015) Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes. The ISME journal 9: 2642, 2656

  50. Suh S-S, Park M, Hwang J, Kil E-J, Jung SW, Lee S, Lee T-K (2015) Seasonal dynamics of marine microbial community in the South Sea of Korea. PLoS One 10, e0131633

  51. Danza F, Ravasi D, Storelli N, Roman S, Lüdin S, Bueche M, Tonolla M (2018) Bacterial diversity in the water column of meromictic Lake Cadagno and evidence for seasonal dynamics. PLoS One 13: e0209743

  52. Baricz A, Chiriac CM, Andrei A-S, Bulzu P-A, Levei EA, Cadar O, Battes KP, Cimpean M, Senila M, Cristea A (2020) Spatio-temporal insights into microbiology of the freshwater-to-hypersaline, oxic-hypoxic-euxinic waters of Ursu Lake. Environ Microbiol

  53. Weber L, Gonzalez-Díaz P, Armenteros M, Apprill A (2019) The coral ecosphere: a unique coral reef habitat that fosters coral–microbial interactions. Limnol Oceanogr 64: 2373–2388

  54. Okamura T, Mori Y, Nakano S-i, Kondo R (2012) Abundance and bacterivory of heterotrophic nanoflagellates in the meromictic Lake Suigetsu, Japan. Aquat Microb Ecol 66: 149–158

  55. Tuomi P, Torsvik T, Heldal M, Bratbak G (1997) Bacterial population dynamics in a meromictic lake. Appl Environ Microbiol 63:2181–2188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Chan Y-F, Chiang K-P, Ku Y, Gong G-C (2019) Abiotic and biotic factors affecting the ingestion rates of mixotrophic nanoflagellates (Haptophyta). Microb Ecol 77:607–615

    Article  PubMed  Google Scholar 

  57. Noguerola I, Picazo A, Llirós M, Camacho A, Borrego CM (2015) Diversity of freshwater Epsilonproteobacteria and dark inorganic carbon fixation in the sulphidic redoxcline of a meromictic karstic lake. Fems Microbiol Ecol 91: fiv086

  58. Rogozin DY, Zykov V, Tarnovskii M (2016) Dynamics of purple sulfur bacteria in a meromictic saline Lake Shunet (Khakassia, Siberia) in 2007–2013. Microbiology 85: 93–101

  59. Benjamini Y, Speed TP (2012) Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res 40:e72–e72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Hoppman-Chaney N, Peterson LM, Klee EW, Middha S, Courteau LK, Ferber MJ (2010) Evaluation of oligonucleotide sequence capture arrays and comparison of next-generation sequencing platforms for use in molecular diagnostics. Clin Chem 56:1297–1306

    Article  CAS  PubMed  Google Scholar 

  61. Jung Y-T, Park S, Lee J-S, Yoon J-H (2016) Loktanella marina sp. nov., isolated from seawater. Int J Syst Evol Microbiol 66:2528–2533

    Article  CAS  PubMed  Google Scholar 

  62. Van Trappen S, Mergaert J, Swings J (2004) Loktanella salsilacus gen. nov., sp. nov., Loktanella fryxellensis sp. nov. and Loktanella vestfoldensis sp. nov., new members of the Rhodobacter group, isolated from microbial mats in Antarctic lakes. Int J Syst Evol Microbiol 54: 1263–1269

  63. Ginzburg B, Chalifa I, Gun J, Dor I, Hadas O, Lev O (1998) DMS formation by dimethylsulfoniopropionate route in freshwater. Environ Sci Technol 32:2130–2136

    Article  CAS  Google Scholar 

  64. Fritz M, Bachofen R (2000) Volatile organic sulfur compounds in a meromictic alpine lake. Acta Hydrochim Hydrobiol 28:185–192

    Article  CAS  Google Scholar 

  65. Gibson JA, Vincent WF, Van Hove P, Belzile C, Wang X, Muir D (2002) Geochemistry of ice-covered, meromictic Lake A in the Canadian High Arctic. Aquat Geochem 8:97–119

    Article  CAS  Google Scholar 

  66. Ohki K, Yamada K, Kamiya M, Yoshikawa S (2009) Morphological, phylogenetic and physiological studies of pico-cyanobacteria isolated from the halocline of a saline meromictic lake, Lake Suigetsu, Japan. Microbes Environ 27:171–178

    Article  Google Scholar 

  67. Kondo R, Kodera M, Mori Y, Okamura T, Yoshikawa S, Ohki K (2014) Spatiotemporal distribution of bacteriochlorophylls in the meromictic Lake Suigetsu, Japan. Limnology 15:77–83

    Article  CAS  Google Scholar 

  68. Labrenz M, Hirsch P (2001) Physiological diversity and adaptations of aerobic heterotrophic bacteria from different depths of hypersaline, heliothermal and meromictic Ekho Lake (East Antarctica). Polar Biol 24

  69. Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454

    Article  CAS  PubMed  Google Scholar 

  70. Prokopkin IG, Zadereev ES (2018) A model study of the effect of weather forcing on the ecology of a meromictic Siberian lake. J Oceanol Limnol 36:2018–2032

    Article  CAS  Google Scholar 

  71. Sorokin DY, Tourova T, Kolganova T, Detkova E, Galinski E, Muyzer G (2011) Culturable diversity of lithotrophic haloalkaliphilic sulfate-reducing bacteria in soda lakes and the description of Desulfonatronum thioautotrophicum sp. nov., Desulfonatronum thiosulfatophilum sp. nov., Desulfonatronovibrio thiodismutans sp. nov., and Desulfonatronovibrio magnus sp. nov. Extremophiles 15: 391–401

  72. Sorokin D, Tourova T, Abbas B, Suhacheva M, Muyzer G (2012) Desulfonatronovibrio halophilus sp. nov., a novel moderately halophilic sulfate-reducing bacterium from hypersaline chloride–sulfate lakes in Central Asia. Extremophiles 16:411–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Overmann J (2001) Diversity and ecology of phototrophic sulfur bacteria. Microbiol Today 28:116–119

    Google Scholar 

  74. Hamilton T, Bovee R, Thiel V, Sattin S, Mohr W, Schaperdoth I, Vogl K, Gilhooly III W, Lyons T, Tomsho L (2014) Coupled reductive and oxidative sulfur cycling in the phototrophic plate of a meromictic lake. Geobiology 12:451–468

    Article  CAS  PubMed  Google Scholar 

  75. Čanković M, Petrić I, Marguš M, Ciglenečki I (2017) Spatio-temporal dynamics of sulfate-reducing bacteria in extreme environment of Rogoznica Lake revealed by 16S rRNA analysis. J Mar Syst 172:14–23

    Article  Google Scholar 

  76. Tonolla M, Peduzzi R, Hahn D (2005) Long-term population dynamics of phototrophic sulfur bacteria in the chemocline of Lake Cadagno, Switzerland. Appl Environ Microbiol 71:3544–3550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ciglenečki I, Ljubešić Z, Janeković I, Batistić M (2017) Rogoznica Lake, a euxinic marine lake on the adriatic coast (Croatia) that fluctuates between anoxic holomictic and meromictic conditions. Ecology of Meromictic Lakes. Springer, pp. 125-154

Download references

Acknowledgments

The authors acknowledge the support from Biodiversity Research Center, Academia Sinica, Taiwan.

Funding

This work was supported by the Russian Foundation for Basic Research (grant no. 19-05-00428) and the Russian Foundation for Basic Research, Government of Krasnoyarsk Territory and Krasnoyarsk Regional Fund of Science (project: «Bottom sediments of Lake Uchum (Krasnoyarsky kray) as a source of information for the reconstruction of the paleo-climate and the prediction of the healing properties of the lake», grant no. 18-45-243002) and the Ministry of Science and Technology, Taiwan (project: “Transition in microbial community of stratified lakes in arid zone of South Siberia: Current and Past,” grant no. 105-2923-B-001-001-MY3 and project: «Postdoctoral Research Fellows», grant no. 108-2811-M-001-603).

Author information

Authors and Affiliations

  1. Biodiversity Research Center, Academia Sinica, Taipei, 115, Taiwan

    Ya-Fan Chan, Pei-Wen Chiang, Kshitij Tandon & Sen-Lin Tang

  2. Bioinformatics Program, Institute of Information Science, Taiwan International Graduate Program, Academia Sinica, Taipei, 115, Taiwan

    Kshitij Tandon

  3. Institute of Molecular and Cellular Biology, National Tsing Hua University, Hsinchu, 300, Taiwan

    Kshitij Tandon

  4. Institute of Biophysics, Siberian Division, Russian Academy of Sciences, Krasnoyarsk, 660036, Russia

    Denis Rogozin, Andrey Degermendzhi & Vladimir Zykov

  5. Siberia Federal University, Krasnoyarsk, 660041, Russia

    Denis Rogozin

Authors
  1. Ya-Fan Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pei-Wen Chiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kshitij Tandon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Denis Rogozin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrey Degermendzhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vladimir Zykov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sen-Lin Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sen-Lin Tang.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic Supplementary Material

ESM 1

(DOCX 13285 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chan, YF., Chiang, PW., Tandon, K. et al. Spatiotemporal Changes in the Bacterial Community of the Meromictic Lake Uchum, Siberia. Microb Ecol 81, 357–369 (2021). https://doi.org/10.1007/s00248-020-01592-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-020-01592-9

Keywords

Search

Navigation