Skip to main content
SpringerLink
Log in

Co-occurrence patterns between phytoplankton and bacterioplankton across the pelagic zone of Lake Baikal during spring

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

Abstract

Phytoplankton and bacterioplankton play a key role in carbon cycling of aquatic ecosystems. In this study, we found that co-occurrence patterns between different types of phytoplankton, bacterioplankton, and environmental parameters in Lake Baikal during spring were different over the course of three consecutive years. The composition of phytoplankton and bacterial communities was investigated using microscopy and 16S rRNA gene pyrosequencing, respectively. Non-metric multidimensional scaling (NMDS) revealed a relationship between the structure of phytoplankton and bacterial communities and temperature, location, and sampling year. Associations of bacteria with diatoms, green microalgae, chrysophyte, and cryptophyte were identified using microscopy. Cluster analysis revealed similar correlation patterns between phytoplankton abundance, number of attached bacteria, ratio of bacteria per phytoplankton cell and environmental parameters. Positive and negative correlations between different species of phytoplankton, heterotrophic bacteria and environmental parameters may indicate mutualistic or competitive relationships between microorganisms and their preferences to the environment.

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

Similar content being viewed by others

References

  • Akaike, H. 1998. Information theory and an extension of the maximum likelihood principle, pp. 199–213. In Selected papers of Hirotugu Akaike, Springer, New York, NY, USA.

    Chapter  Google Scholar 

  • Amin, S.A., Parker, M.S., and Armbrust, E.V. 2012. Interactions between diatom and bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azam, F. and Malfatti, F. 2007. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791.

    Article  CAS  PubMed  Google Scholar 

  • Baker, G.C., Smith, J.J., and Cowan, D.A. 2003. Review and re-analysis of domain-specific 16S primers. J. Microbiol. Methods 55, 541–555.

    Article  CAS  PubMed  Google Scholar 

  • Benjamini, Y. and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300.

    Google Scholar 

  • Bidle, K.D. and Azam, F. 1999. Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature 397, 508–512.

    Article  CAS  Google Scholar 

  • Bidle, K.D. and Azam, F. 2001. Bacterial control of silicon regeneration from diatom detritus: Significance of bacterial ectohydrolases and species identity. Limnol. Oceanogr. 46, 1606–1623.

    Article  CAS  Google Scholar 

  • Buchan, A., Le Cleir, G.R., Gulvik, C.A., and González, J.M. 2014. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat. Rev. Microbiol. 12, 686–698.

    Article  CAS  PubMed  Google Scholar 

  • Bunse, C., Bertos-Fortis, M., Sassenhagen, I., Sildever, S., Sjöqvist, C., Godhe, A., Gross, S., Kremp, A., Lips, I., Lundholm, N., et al. 2016. Spatio-temporal interdependence of bacteria and phytoplankton during a Baltic Sea spring bloom. Front. Microbiol. 7, 1–10.

    Article  Google Scholar 

  • Csardi, G. and Nepusz, T. 2006. The igraph software package for complex network research. Int. J. Complex Syst. 1695, 1–9.

    Google Scholar 

  • Domysheva, V.M., Usoltseva, M.V., Sakirko, M.V., Pestunov, D.A., Shimaraev, M.N., Popovskaya, G.I., and Panchenko, M.V. 2014. Spatial distribution of carbon dioxide fluxes, biogenic elements, and phytoplankton biomass in the pelagic zone of Lake Baikal in spring period of 2010–2012. Atmos. Ocean. Opt. 27, 529–535.

    Article  CAS  Google Scholar 

  • Eiler, A., Heinrich, F., and Bertilsson, S. 2012. Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J. 6, 330–342.

    Article  CAS  PubMed  Google Scholar 

  • Faust, K. and Raes, J. 2012. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10, 538–550.

    Article  CAS  PubMed  Google Scholar 

  • Fogg, G.E. 1983. The ecological significance of extracellular products of phytoplankton photosynthesis. Bot. Mar. 26, 3–14.

    Article  CAS  Google Scholar 

  • Fortunato, C.S., Eiler, A., Herfort, L., Needoba, J.A., Peterson, T.D., and Crump, B.C. 2013. Determining indicator taxa across spatial and seasonal gradients in the Columbia River coastal margin. ISME J. 7, 1899–1911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuhrman, J.A. 2009. Microbial community structure and its functional implications. Nature 459, 193–199.

    Article  CAS  PubMed  Google Scholar 

  • Gärdes, A., Iversen, M.H., Grossart, H.P., Passow, U., and Ulrich, M.S. 2011. Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii. ISME J. 5, 436–445.

    Article  CAS  PubMed  Google Scholar 

  • Gilbert, J.A., Steele, J.A., Caporaso, J.G., Steinbrück, L., Reeder, J., Temperton, B., Huse, S., McHardy, A.C., Knight, R., Joint, I., et al. 2012. Defining seasonal marine microbial community dynamics. ISME J. 6, 298–308.

    Article  CAS  PubMed  Google Scholar 

  • Grossart, H.P., Levold, F., Allgaier, M., Simon, M., and Brinkhoff, T. 2005. Marine diatom species harbour distinct bacterial communities. Environ. Microbiol. 7, 860–873.

    Article  CAS  PubMed  Google Scholar 

  • Hollander, M. and Wolfe, D.A. 1973. Nonparametric statistical methods. John Wiley & Sons, New York, USA.

    Google Scholar 

  • Khodzher, T.V., Domysheva, V.M., Sorokovikova, L.M., Sakirko, M.V., and Tomberg, I.V. 2017. Current chemical composition of Lake Baikal water. Inland Waters 7, 250–258.

    Article  CAS  Google Scholar 

  • Mayali, X. and Azam, F. 2004. Algicidal bacteria in the sea and their impact on algal blooms. J. Eukaryot. Microbiol. 51, 139–144.

    Article  PubMed  Google Scholar 

  • Mayali, X., Franks, P.J.S., and Burton, R.S. 2011. Temporal attachment dynamics by distinct bacterial taxa during a dinoflagellate bloom. Aquat. Microb. Ecol. 63, 111–122.

    Article  Google Scholar 

  • Mikhailov, I.S., Zakharova, Y.R., Bukin, Y.S., Galachyants, Y.P., Petrova, D.P., Sakirko, M.V., and Likhoshway, Y.V. 2019. Cooccurrence networks among bacteria and microbial eukaryotes of Lake Baikal during a spring phytoplankton bloom. Microb. Ecol. 77, 96–109.

    Article  PubMed  Google Scholar 

  • Mikhailov, I.S., Zakharova, Y.R., Galachyants, Y.P., Usoltseva, M.V., Petrova, D.P., Sakirko, M.V., Likhoshway, Y.V., and Grachev, M.A. 2015. Similarity of structure of taxonomic bacterial communities in the photic layer of Lake Baikal’s three basins differing in spring phytoplankton composition and abundance. Dokl. Biochem. Biophys. 465, 413–419.

    Article  CAS  PubMed  Google Scholar 

  • 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., et al. 2016. Vegan: Community ecology package. version 2.4-1. https://doi.org/CRAN.R-project.org/package=vegan.

    Google Scholar 

  • Paver, S.F., Hayek, K.R., Gano, K.A., Fagen, J.R., Brown, C.T., Davis-Richardson, A.G., Grabb, D.B., Rosario-Passapera, R., Giongo, A., Triplett, E.W., et al. 2013. Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. Environ. Microbiol. 15, 2489–2504.

    Article  PubMed  Google Scholar 

  • Pearman, J.K., Casas, L., Merle, T., Michell, C., and Irigoien, X. 2015. Bacterial and protist community changes during a phytoplankton bloom. Limnol. Oceanogr. 61, 198–213.

    Article  Google Scholar 

  • Pomazkina, G.V., Belykh, O.I., Domysheva, V.M., Sakirko, M.V., and Gnatovskii, R.Y. 2010. Structure and dynamics of the phytoplankton in Southern Baikal (Russia). Int. J. Algae 12, 64–79.

    Article  CAS  Google Scholar 

  • Popovskaya, G.I., Usol’tseva, M.V., Domysheva, V.M., Sakirko, M.V., Blinov, V.V., and Khodzher, T.V. 2015. The spring phytoplankton in the pelagic zone of Lake Baikal during 2007–2011. Geogr. Nat. Resour. 36, 253–262.

    Article  Google Scholar 

  • Porter, K.G. and Feig, Y.S. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25, 943–948.

    Article  Google Scholar 

  • Quince, C., Lanzen, A., Davenport, R.J., and Turnbaugh, P.J. 2011. Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12, 1–18.

    Article  Google Scholar 

  • Rooney-Varga, J.N., Giewat, M.W., Savin, M.C., Sood, S., LeGresley, M., and Martin, J.L. 2005. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb. Ecol. 49, 163–175.

    Article  CAS  PubMed  Google Scholar 

  • Royston, P. 1995. Remark AS R94: a remark on algorithm AS 181: the W-test for normality. J. R. Stat. Soc. Ser. C Appl. Stat. 44, 547–551.

    Google Scholar 

  • Rösel, S. and Grossart, H.P. 2012. Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring. Aquat. Microb. Ecol. 66, 169–181.

    Article  Google Scholar 

  • Sarmento, H. and Gasol, J.M. 2012. Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Environ. Microbiol. 14, 2348–2360.

    Article  CAS  PubMed  Google Scholar 

  • Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., et al. 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 

  • Shimaraev, M.N., Verbolov, V.I., Granin, N.G., and Sherstayankin, P.P. 1994. Physical limnology of Lake Baikal: a review. Baikal Int. Center for Ecological Research, Irkutsk Okayama, Japan.

    Google Scholar 

  • Sison-Mangus, M.P., Jiang, S., Tran, K.N., and Kudela, R.M. 2014. Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota. ISME J. 8, 63–76.

    Article  CAS  PubMed  Google Scholar 

  • Smith, E.P. and van Belle, G. 1984. Nonparametric estimation of species richness. Biometrics 40, 119–129.

    Article  Google Scholar 

  • Smriga, S., Fernandez, V.I., Mitchell, J.G., and Stocker, R. 2016. Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc. Natl. Acad. Sci. USA 113, 1576–1581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki, R. and Shimodaira, H. 2006. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540–1542.

    Article  CAS  PubMed  Google Scholar 

  • Tan, S., Zhou, J., Zhu, X., Yu, S., Zhan, W., Wang, B., and Cai, Z. 2015. An association network analysis among microeukaryotes and bacterioplankton reveals algal bloom dynamics. J. Phycol. 51, 120–132.

    Article  CAS  PubMed  Google Scholar 

  • Teeling, H., Fuchs, B.M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C.M., Kassabgy, M., Huang, S., Mann, A.J., Waldmann, J., et al. 2012. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608–611.

    Article  CAS  PubMed  Google Scholar 

  • Teeling, H., Fuchs, B.M., Bennke, C.M., Krüger, K., Chafee, M., Kappelmann, L., Reintjes, G., Waldmann, J., Quast, C., Glöckner, F.O., et al. 2016. Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms. Elife 5, e11888.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vacher, C., Tamaddoni-Nezhad, A., Kamenova, S., Peyrard, N., Moalic, Y., Sabbadin R., Schwaller, L., Chiquet, J., Smith, M.A., Vallance, J., et al. 2016. Chapter one-learning ecological networks from next-generation sequencing data. Adv. Ecol. Res. 54, 1–39.

    Article  Google Scholar 

  • Warnes, G.R., Bolker, B., Bonebakker, L., Gentleman, R., Huber, W., Liaw, W.H.A., Lumley, T., Maechler, M., Magnusson, A., Moeller, S., et al. 2009. Gplots: Various R programming tools for plotting data. R package version 2.4.

    Google Scholar 

  • Weiss, S., Van Treuren, W., Lozupone, C., Faust, K., Friedman, J., Deng, Y., Xia, L.C., Xu, Z.Z., Ursell, L., Alm, E.J., et al. 2016. Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J. 10, 1669–1681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakharova, Y.R., Adel’shin, R.V., Parfenova, V.V., Bedoshvili, Y.D., and Likhoshway, Y.V. 2010. Taxonomic characterization of the microorganisms associated with the cultivable diatom Synedra acus from Lake Baikal. Microbiology 79, 679–687.

    Article  CAS  Google Scholar 

  • Zakharova, Y.R., Galachyants, Y.P., Kurilkina, M.I., Likhoshvay, A.V., Petrova, D.P., Shishlyannikov, S.M., Ravin, N.V., Mardanov, A.V., Beletsky, A.V., and Likhoshway, Y.V. 2013. The structure of microbial community and degradation of diatoms in the deep near-bottom layer of Lake Baikal. PLoS One 8, e59977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., Wang, K., Shen, L., Chen, H., Hou, F., Zhou, X., Zhang, D., and Zhu, X. 2018. Microbial community dynamics and assembly follows trajectories of an early spring diatom bloom in a semi-enclosed bay. Appl. Environ. Microbiol. 84, e01000–18.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Znachor, P., Simek, K., and Nedoma, J. 2012. Bacterial colonization of the freshwater planktonic diatom Fragilaria crotonensis. Aquat. Microb. Ecol. 66, 87–94.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Limnological Institute, Siberian Branch of the Russian Academy of Sciences, Irkutsk, Russia

    Ivan S. Mikhailov, Yuri S. Bukin, Yulia R. Zakharova, Marina V. Usoltseva, Yuri P. Galachyants, Maria V. Sakirko, Vadim V. Blinov & Yelena V. Likhoshway

  2. Irkutsk Scientific Center, Siberian Branch of the Russian Academy of Sciences, Irkutsk, Russia

    Ivan S. Mikhailov, Yuri S. Bukin, Yulia R. Zakharova, Yuri P. Galachyants & Yelena V. Likhoshway

Authors
  1. Ivan S. Mikhailov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuri S. Bukin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yulia R. Zakharova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marina V. Usoltseva
    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. Maria V. Sakirko
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vadim V. Blinov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yelena V. Likhoshway
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ivan S. Mikhailov.

Additional information

Supplemental material for this article may be found at https://doi.org/www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mikhailov, I.S., Bukin, Y.S., Zakharova, Y.R. et al. Co-occurrence patterns between phytoplankton and bacterioplankton across the pelagic zone of Lake Baikal during spring. J Microbiol. 57, 252–262 (2019). https://doi.org/10.1007/s12275-019-8531-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-019-8531-y

Keywords

Search

Navigation