Skip to main content
SpringerLink
Log in

Sub-Ice Microalgal and Bacterial Communities in Freshwater Lake Baikal, Russia

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

Abstract

The sub-ice environment of Lake Baikal represents a special ecotope where strongly increasing microbial biomass causes an “ice-bloom” contributing therefore to the ecosystem functioning and global element turnover under low temperature in the world’s largest freshwater lake. In this work, we analyzed bacterial and microalgal communities and their succession in the sub-ice environment in March–April 2010–2012. It was found out that two dinoflagellate species (Gymnodinium baicalense var. minor and Peridinium baicalense Kisselew et Zwetkow) and four diatom species (Aulacoseira islandica, A. baicalensis, Synedra acus subsp. radians, and Synedra ulna) predominated in the microalgal communities. Interestingly, among all microalgae, the diatom A. islandica showed the highest number of physically attached bacterial cells (up to 67 ± 16 bacteria per alga). Bacterial communities analyzed with pyrosequencing of 16S rRNA gene fragments were diverse and represented by 161 genera. Phyla Proteobacteria, Verrucomicrobia, Actinobacteria, Acidobacteria, Bacteroidetes, and Cyanobacteria represented a core community independently on microalgal composition, although the relative abundance of these bacterial phyla strongly varied across sampling sites and time points; unique OTUs from other groups were rare.

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
Fig. 8

Similar content being viewed by others

References

  1. Galazy GI (1993) Atlas of Lake Baikal. Ruscartography, Moscow

    Google Scholar 

  2. Shimaraev MN, Verbolov VI, Granin NG, Sherstyankin PP (1994) Physical Limnology of Lake Baikal: A review. BICER Publishers, 81 pp

  3. Livingston DW (1999) Ice break-up on southern Lake Baikal and its relationship to local and regional air temperatures in Siberia and to the North Atlantic Oscillation. Limnol Oceanogr 44:1486–1497

    Article  Google Scholar 

  4. Magnuson JJ et al (2000) Historical trends in lake and river ice cover in the northern hemisphere. Science 289:1743–1747

    Article  CAS  PubMed  Google Scholar 

  5. Shimaraev MN (1971) Hydrometeorological factors and oscillations of Baikal plankton abundance. In: Limnology of Pre-delta areas of Lake Baikal. Nauka, Leningrad, pp 259–267

  6. Granin NG, Jewson DH, Gnatovsky RY, Levin LA, Zhdanov AA, Gorbunova LA, Tsekhanovsky VV, Doroschenko LM, Mogilev NY (2000) Turbulent mixing under ice and the growth of diatoms in Lake Baikal. Verh Internat Verein Limnol 27:2812–2814

    Google Scholar 

  7. Jewson DH, Granin NG, Zhdanov AA, Gnatovsky RY (2009) Effect of snow depth on under-ice irradiance and growth of Aulacoseira baicalensis in Lake Baikal. Aquat Ecol 43:673–679. doi:10.1007/s10452-009-9267-2

    Article  CAS  Google Scholar 

  8. Meguro H, Ito K, Fukushima H (1967) Ice flora (bottom type): a mechanism of primary production in polar seas and the growth of diatoms in sea ice. Arctic 20(2):114–133

    Article  Google Scholar 

  9. Cota GF, Legendre L, Gosselin M, Ingram RG (1991) Ecology of bottom ice algae: I. Environmental controls and variability. J Mar Syst 2:257–277

    Article  Google Scholar 

  10. Gutt J (1995) The occurrence of sub-ice algal aggregations off northeast Greenland. Polar Biol 15:247–252

    Article  Google Scholar 

  11. Gradinger R (1996) Occurrence of an algal bloom under Arctic pack ice. Mar Ecol Prog Ser 131:301–305

    Article  Google Scholar 

  12. Ambrose WG, Quillfeldt C, Clough LM, Tilney PVR, Tucker T (2005) The sub-ice algal community in the Chukchi sea: large- and small-scale patterns of abundance based on images from a remotely operated vehicle. Polar Biol 28:784–795. doi:10.1007/s00300-005-0002-8

    Article  Google Scholar 

  13. Poulin M, Underwood GJC, Michel C (2014) Sub-ice colonial Melosira arctica in Arctic first-year ice. Diatom Research. doi:10.1080/0269249X.2013.877085

    Google Scholar 

  14. Bunch JN, Harland RC (1990) Bacterial production in the bottom surface of sea Canadian Subarctic. Can J Aquat Sci 47:1986–1995

    Article  Google Scholar 

  15. Spilling K (2007) Dense sub-ice bloom of dinoflagellates in the Baltic Sea, potentially limited by high pH. J Plankton Res 29(10):895–901. doi:10.1093/plankt/fbm067

    Article  CAS  Google Scholar 

  16. Różańska M, Gosselin M, Poulin M, Wiktor JM, Michel C (2009) Influence of environmental factors on the development of bottom ice protist communities during the winter–spring transition. Mar Ecol Prog Ser 386:43–59. doi:10.3354/meps08092

    Article  Google Scholar 

  17. Horner RA, Ackley SF, Dieckmann GS, Gulliksen B, Hoshiai T, Legender L, Melnikov IA, Reeburgh WS, Spindler M, Sullivan CW (1992) Ecology of sea ice biota. Polar Biol 12:417–427

    Article  Google Scholar 

  18. Skabitchevsky AP (1929) On the biology of Melosira baicalensis (K. Meyer) Wisl. Rus Hydrobiol Zh 8:93–114

    Google Scholar 

  19. Yasnitsky VN (1930) Results on observations of Baikal plankton in the region of Biological Station during 1926-1928. News Biol Geographic Institute Irkutsk State Univ 4(3-4):191–234

    Google Scholar 

  20. Izmest’eva LR, Moore MV, Hampton SE (2006) Seasonal dynamics of common phytoplankton in Lake Baikal. Proc Samara RAS (Russian Acad Sci) Sci Centre 8(3):191–196

    Google Scholar 

  21. Obolkina LA, Bondarenko NA, Doroschenko LF, Gorbunova LA, Molozhavaya OA (2000) About finding of cryophilic communities in Lake Baikal. Dokl Akad Nauk 371:815–817 (In Russian)

    CAS  Google Scholar 

  22. Bondarenko NA, Timoshkin OA, Röpstorf P, Melnik NG (2006) The under-ice and bottom periods in the life of Aulacoseira baicalensis (K. Meyer) Simonsen, a principal Lake Baikal alga. Hydrobiologia 568:107–109. doi:10.1007/s10750-006-0325-7

    Article  Google Scholar 

  23. Bedoshvili EL, Bondarenko NA, Sakirko MV, Khanaev IV, Likhoshway EV (2007) Changes of colony length in the planktonic diatom Aulacoseira baicalensis at different stages of its annual cycle in Lake Baikal. Hydrobiol J 43(3):81–89

    Google Scholar 

  24. Jewson DH, Granin NG, Zhdarnov AA, Gorbunova LA, Bondarenko NA, Gnatovsky RY (2008) Resting stages and ecology of the planktonic diatom Aulacoseira skvortzowii in Lake Baikal. Limnol Oceanog 53:1125–1136

    Article  Google Scholar 

  25. Jewson DH, Granin NG, Zhdarnov AA, Gorbunova LA, Gnatosvsky RY (2010) Vertical mixing, size changes and resting stage formation of the planktonic diatom Aulacosira baicalensis. Eur J Phycol 45:354–364. doi:10.1080/09670262.2010.492915

    Article  Google Scholar 

  26. Kozhova OM, Izmest’eva LR (1998) Lake Baikal: evolution and biodiversity. Backhuys Publ, Leiden

    Google Scholar 

  27. Pomazkina GV, Belykh OI, Domysheva VM, Sakirko MV, Gnatovsky RY (2010) Structure and dynamics of phytoplankton of Southern Baikal (Russia). Inter J Algae 12(1):64–79. doi:10.1615/InterJAlgae.v12.i1.50

    Article  CAS  Google Scholar 

  28. Annenkova NV (2013) Phylogenetic relations of the dinoflagellate Gymnodinium baicalense from Lake Baikal. Cent Eur J Biol 8(4):366–373. doi:10.2478/s11535-013-0144-y

    Google Scholar 

  29. Werner I (1997) Grazing of Arctic under-ice amphipods on sea-ice. Mar Ecol Prog Ser 160:93–99

    Article  Google Scholar 

  30. Werner I, Arbizu PM (1999) The sub-ice fauna of the Laptev Sea and the adjacent Arctic Ocean in summer 1995. Polar Biol 21:71–79

    Article  Google Scholar 

  31. Jeong (1999) The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J Eukrmor Microbiol 46(4):390–396

    Article  Google Scholar 

  32. Levinsen H, Nielsen TG (2002) The trophic role of marine pelagic ciliates and heterotrophic dinoflagellates in arctic and temperate coastal ecosystems: a cross-latitude comparison. Limnol Oceanogr 47(2):427–439

    Article  Google Scholar 

  33. Straškrábová V, Izmest’yeva LR, Maksimova EA, Fietz S, Nedoma J, Borovec J, Kobanova GI, Shchetinina EV, Pislegina EV (2005) Primary production and microbial activity in the euphotic zone of Lake Baikal (Southern Basin) during late winter. Glob Planet Chang 46:57–73. doi:10.1016/j.gloplacha.2004.11.006

    Article  Google Scholar 

  34. Ahn T, Hong S, Kim D, Suck J, Drucker VV (1999) The bacterial community of Southern Lake Baikal in winter. J Microbiol 37(1):10–13

    Google Scholar 

  35. D’souza NA, Kawarasaki Y, Gantz JD, Lee JRE, Beall BFN, Shtarkman YM, Koçer ZA, Rogers SO, Wildschutte H, Bullerjahn GS, McKay RML (2013) Diatom assemblages promote ice formation in large lakes. ISME J 7:1632–1640

    Article  PubMed Central  PubMed  Google Scholar 

  36. McConville MJ, Wetherbee R (1983) The bottom-ice microalgal community from annual ice in the inshore waters of East Antarctica. J Phycol 19:431–439

    Article  Google Scholar 

  37. Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microb 63(8):3068–3078

    CAS  Google Scholar 

  38. Smith REH, Clement P, Cota GF (1989) Population dynamics of bacteria in Arctic Sea Ice. Microb Ecol 17:63–76

    Article  CAS  PubMed  Google Scholar 

  39. Rooney-Varga JN, Giewat MW, Savin MC, Sood S, LeGresley M, Martin JL (2005) Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb Ecol 49:163–175. doi:10.1007/s00248-003-1057-0d

    Article  CAS  PubMed  Google Scholar 

  40. Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrase C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microb 70(11):6753–6766. doi:10.1128/AEM.70.11.6753-6766.2004

    Article  CAS  Google Scholar 

  41. Sapp M, Schwaderer AS, Wiltshire KH, Hoppe H, Gerdts G, Wichels A (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol 53:683–699. doi:10.1007/s00248-006-9162-5

    Article  PubMed  Google Scholar 

  42. Schäfer H, Abbas B, Witte H, Muyzer G (2002) Genetic diversity of ‘satellite’ bacteria present in cultures of marine diatoms. FEMS Microbiol Ecol 42:25–35

    PubMed  Google Scholar 

  43. Grossart H-P, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7(6):860–873

    Article  CAS  PubMed  Google Scholar 

  44. Rusinek OT, Takhteev VV, Gladkochub DP, Khodzher TV, Budnev NM et al. (2012) Baikal Science Vol 1. Nauka, Novosibirsk

  45. Sadchikov AP (2003) Methods for studying freshwater phytoplankton. “University and School”, Moscow

  46. Wetzel RG, Likens GE (1991) Limnological analyses. Springer-Verlag, New York

    Book  Google Scholar 

  47. Stroganov NS, Buzinova NS (1980) A Practical guide to the hydrochemistry. Moscow University Press, Moscow

    Google Scholar 

  48. Belykh OI, Bessudova AY, Gladkikh AS, Kuzmina AE, Pomazkina GV, Popovskaya GI, Sorokovikova EG, Tikhonova IV, Usoltseva MV, Firsova AD, Likhoshway EV (2011) Manual for estimation of phytoplankton biomass in the Lake Baikal pelagic zone. ISU, Irkutsk

    Google Scholar 

  49. Popovskaya GI, Genkal SI, Likhoshway EV (2011) Diatoms in the Lake Baikal plankton, Atlas-Key. Nauka, Novosibirsk

    Google Scholar 

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

    Google Scholar 

  51. Makarova IV, Pichkily LO (1970) To some problems on techniques of phytoplankton biomass estimation. Botanic J 55(10):1488–1494

    Google Scholar 

  52. Wetzel RG, Likens GE (2000) Composition and biomass of phytoplankton. In: Limnological analyses. Springer Verlag, New York, pp 147–174. doi: 10.1007/978-1-4757-3250-4_10

  53. Zakharova YR, Adel’shin RV, Parfenova VV, Bedoshvili YD, Likhoshway YV (2010) Taxonomic characterization of microorganisms associated with cultured diatoms Synedra acus from Lake Baikal. Microbiology 79(5):679–687. doi:10.1134/S0026261710050139

    Article  CAS  Google Scholar 

  54. Gerhardt P, Costilow RN, Krieg NR, Murrey RGE, Nester EW, Phillips GB, Wood WA (1981) Manual of methods for general bacteriology. Amer Soc Microbiol, Washington

    Google Scholar 

  55. Zakharova YR, Galachyants YP, Kurilkina MI, Likhoshvay AV, Petrova DP et al (2013) The structure of microbial community and degradation of diatoms in the deep near-bottom layer of Lake Baikal. PLoS ONE 8(4), e59977. doi:10.1371/journal.pone.0059977

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. Gumerov VM, Mardanov AV, Beletsky AV, Bonch-Osmolovskaya EA, Ravin NV (2011) Molecular analysis of microbial diversity in the Zavarzin Spring, Uzon Caldera, Kamchatka. Microbiology 80(2):244–251. doi:10.1134/S002626171102007X

    Article  CAS  Google Scholar 

  57. 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 Microb 75:7537–7541. doi:10.1128/AEM.01541-09

    Article  CAS  Google Scholar 

  58. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinf 12(38):1–18

    Google Scholar 

  59. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. doi:10.1093/bioinformatics/btr381

    PubMed Central  PubMed  Google Scholar 

  60. Cole JR, Wang Q, Cardenas E, Fish J, Chai B (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:141–145. doi:10.1093/nar/gkn879

    Article  Google Scholar 

  61. Golobokova LP, Sakirko MV, Onischuk NA, Pogodaeva TV, Sez`ko NP, Dolya IN (2009) Hydrochemical characteristic of littoral waters of north-western coast of Southern Baikal. In: Timoshkin OA (ed) Index of animal species inhabiting Lake Baikal and its catchment area, vol 2. Nauka, Novosibirsk, pp 760–784

    Google Scholar 

  62. Ji X, Han X, Zheng L, Yang B, Yu Z, Zou J (2011) Allelopathic interactions between Prorocentrum micans and Skeletonema costatum or Karenia mikimotoi in laboratory cultures. Chin J Oceanol Limn 29(4):840–848. doi:10.1007/s00343-011-0512-x

    Article  Google Scholar 

  63. Wang J, Zhang Y, Li H, Cao J (2013) Competitive interaction between diatoms Skeletonema costatum and dinoflagellate Prorocentrum donghaiense in laboratory culture. J Plankton Res 35(2):367–378. doi:10.1093/plankt/fbs098

    Article  CAS  Google Scholar 

  64. Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Ann Rev Ecol Syst 13:291–314

    Article  Google Scholar 

  65. Arrigo KR (2014) Sea ice ecosystems. Annu Rev Mar Sci 6:13.1–13.29. doi:10.1146/annurev-marine-010213-135103

    Article  Google Scholar 

  66. Riquelm CE, Fukami K, Ishida Y (1988) Effects of bacteria on the growth of diatom, Asterionella gracialis. B Jpn Soc Microb Ecol 3(1):29–34

    Google Scholar 

  67. Vieira AAH, Giroldo D, Ortolan PIC (2006) Aggregate formation in axenic and microbial co-inoculated batch cultures of Aulacoseira granulata (Bacillariophyceae). Acta Limnol Bras 18(1):1–7

    Google Scholar 

  68. Parveen B, Reveilliez J-P, Mary I, Ravet V, Bronner G, Mangot J-F, Domaizon I, Debroas D (2011) Diversity and dynamics of free-living and particle-associated Betaproteobacteria and Actinobacteria in relation to phytoplankton and zooplankton communities. FEMS Microbiol Ecol 77:461–476. doi:10.1111/j.1574-6941.2011.01130.x

    Article  CAS  PubMed  Google Scholar 

  69. Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol R 76(3):667–684. doi:10.1128/MMBR.00007-12

    Article  CAS  Google Scholar 

  70. Bagatini IL, Eiler A, Bertilsson S, Klaveness D, Tessarolli LP et al (2014) Host-specificity and dynamics in bacterial communities associated with bloom-forming freshwater phytoplankton. PLoS ONE 9(1), e85950. doi:10.1371/journal.pone.0085950

    Article  PubMed Central  PubMed  Google Scholar 

  71. Jiang F, Li W, Xiao M, Dai J, Kan W, Chen L, Li W, Fang C, Peng F (2012) Luteolibacter luojiensis sp. nov., isolated from Arctic tundra soil, and emended description of the genus Luteolibacter. Int J Syst Evol Microbiol 62:2259–2263. doi:10.1099/ijs.0.037309-0

    Article  CAS  PubMed  Google Scholar 

  72. Stoermer EF, Kreis RG, Sicko-Goad J, Sicko-Goad L (1981) A systematic, quantitative and ecological comparison of Melosira islandica O. Müll. with M. granulata (EHR.) ralfs from the Laurentian Great Lakes. J Great Lakes Res 7(4):345–356

    Article  Google Scholar 

  73. Garrity GM (2005) Bergey’s manual of systematic bacteriology I–II. Springer Verlag, New York

    Google Scholar 

  74. Votintsev KK, Meshcheryakova AI, Popovskaya GI (1975) Cycle of organic matter in Lake Baikal. Nauka, Novosibirsk

    Google Scholar 

  75. Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microb 70(1):202–213. doi:10.1128/AEM.70.1.202-213.2004

    Article  CAS  Google Scholar 

  76. Parfenova VV, Gladkikh AS, Belykh OI (2013) Comparative analysis of biodiversity in the planktonic and biofilm bacterial communities in Lake Baikal. Microbiology 82(1):91–101. doi:10.1134/S0026261713010128

    Article  CAS  Google Scholar 

  77. Kadnikov VV, Mardanov AV, Beletsky AV, Shubenkova OV, Pogodaeva TV (2012) Microbial community structure in methane hydrate-bearing sediments of freshwater Lake Baikal. FEMS Microbiol Ecol 79:348–358. doi:10.1111/j.1574-6941.2011.01221.x

    Article  CAS  PubMed  Google Scholar 

  78. Jing H, Xia X, Suzuki K, Liu H (2013) Vertical profiles of bacteria in the tropical and subarctic oceans revealed by pyrosequencing. PLoS ONE 8(11), e79423. doi:10.1371/journal.pone.0079423

    Article  PubMed Central  PubMed  Google Scholar 

  79. An S, Couteau C, Luo F, Neveu J, DuBow MS (2013) Bacterial diversity of surface sand samples from the Gobi and Taklamaken deserts. Microb Ecol 66:850–860. doi:10.1007/s00248-013-0276-2

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the interdisciplinary integrated projects of the Siberian Branch of the Russian Academy of Science # 137 (sequencing) and projects of Federal Agency of Scientific Organizations # VI.61.1.4 (data analysis). The authors are thankful to A. Kupchinsky, N. Volokitina, S. Shishlyannikov, and I. Mikhailov (Limnological Institute) for their assistance in sampling; M. Sakirko and V. Domysheva for chemical analysis; M. Shimaraev for consultation on hydrophysics; T. Zemskaya for insightful comments and suggestions; and to G. Nagornaya and N. Gorgolyuk for English translation.

Author information

Authors and Affiliations

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

    Maria V. Bashenkhaeva, Yulia R. Zakharova, Darya P. Petrova, Igor V. Khanaev, Yuri P. Galachyants & Yelena V. Likhoshway

Authors
  1. Maria V. Bashenkhaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yulia R. Zakharova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Darya P. Petrova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Igor V. Khanaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuri P. Galachyants
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yelena V. Likhoshway
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria V. Bashenkhaeva.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 2.07 MB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bashenkhaeva, M.V., Zakharova, Y.R., Petrova, D.P. et al. Sub-Ice Microalgal and Bacterial Communities in Freshwater Lake Baikal, Russia. Microb Ecol 70, 751–765 (2015). https://doi.org/10.1007/s00248-015-0619-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0619-2

Keywords

Search

Navigation