Microbial Ecology

, Volume 77, Issue 1, pp 96–109 | Cite as

Co-occurrence Networks Among Bacteria and Microbial Eukaryotes of Lake Baikal During a Spring Phytoplankton Bloom

  • Ivan S. MikhailovEmail author
  • Yulia R. Zakharova
  • Yuri S. Bukin
  • Yuri P. Galachyants
  • Darya P. Petrova
  • Maria V. Sakirko
  • Yelena V. Likhoshway
Environmental Microbiology


The pelagic zone of Lake Baikal is an ecological niche where phytoplankton bloom causes increasing microbial abundance in spring which plays a key role in carbon turnover in the freshwater lake. Co-occurrence patterns revealed among different microbes can be applied to predict interactions between the microbes and environmental conditions in the ecosystem. We used 454 pyrosequencing of 16S rRNA and 18S rRNA genes to study bacterial and microbial eukaryotic communities and their co-occurrence patterns at the pelagic zone of Lake Baikal during a spring phytoplankton bloom. We found that microbes within one domain mostly correlated positively with each other and are highly interconnected. The highly connected taxa in co-occurrence networks were operational taxonomic units (OTUs) of Actinobacteria, Bacteroidetes, Alphaproteobacteria, and autotrophic and unclassified Eukaryota which might be analogous to microbial keystone taxa. Constrained correspondence analysis revealed the relationships of bacterial and microbial eukaryotic communities with geographical location.


Co-occurrence network Bacteria Microbial eukaryotes Community Lake Baikal Pyrosequencing 



We thank R.Yu. Gnatovsky and V.V. Blinov from the hydrology and hydrophysics laboratory of Limnological Institute of SB RAS for collecting water samples and providing temperature data.

Funding information

This work was supported by the Federal Agency of Scientific Organizations (FASO) of Russia under the subject No. 0345-2016-0005 (pyrosequencing results) and the subject No. 0345-2016-0001 (metagenomic and statistical analyzes).

Supplementary material

248_2018_1212_MOESM1_ESM.doc (4.8 mb)
ESM 1 (DOC 4902 kb)


  1. 1.
    Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thébault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538. CrossRefPubMedGoogle Scholar
  2. 2.
    Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696CrossRefGoogle Scholar
  3. 3.
    Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791. CrossRefPubMedGoogle Scholar
  4. 4.
    Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199. CrossRefGoogle Scholar
  5. 5.
    Buchan A, LeCleir GR, Gulvik CA, González JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698. CrossRefPubMedGoogle Scholar
  6. 6.
    Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Martiny JBH, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. CrossRefPubMedGoogle Scholar
  8. 8.
    Jones AC, Liao TSV, Najar FZ, Roe BA, Hambright KD, Caron DA (2013) Seasonality and disturbance: annual pattern and response of the bacterial and microbial eukaryotic assemblages in a freshwater ecosystem. Environ Microbiol 15:2557–2572. CrossRefPubMedGoogle Scholar
  9. 9.
    Smith MW, Allen LZ, Allen AE, Herfort L, Simon HM (2013) Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem. Front Microbiol 4:1–20. CrossRefGoogle Scholar
  10. 10.
    Andersson AF, Riemann L, Bertilsson S (2010) Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J 4:171–181. CrossRefPubMedGoogle Scholar
  11. 11.
    Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glockner FO, Schweder T, Amann R (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611. CrossRefPubMedGoogle Scholar
  12. 12.
    Bunse C, Bertos-Fortis M, Sassenhagen I, Sildever S, Sjӧqvist C, Godhe A, Gross S, Kremp A, Lips I, Lundholm N, Rengefors K, Sefbom J, Pinhassi J, Legrand C (2016) Spatio-temporal interdependence of bacteria and phytoplankton during a Baltic Sea spring bloom. Front Microbiol 7:1–10. CrossRefGoogle Scholar
  13. 13.
    Rӧsel S, Grossart HP (2012) Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring. Aquat Microb Ecol 66:169–181. CrossRefGoogle Scholar
  14. 14.
    Paver SF, Hayek KR, Gano KA, Fagen JR, Brown CT, Davis-Richardson AG, Grabb DB, Rosario-Passapera R, Giongo A, Triplett EW, Kent AD (2013) Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. Environ Microbiol 15:2489–2504. CrossRefPubMedGoogle Scholar
  15. 15.
    Eiler A, Heinrich F, Bertilsson S (2012) Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6:330–342. CrossRefGoogle Scholar
  16. 16.
    Pearman JK, Casas L, Merle T, Michell C, Irigoien X (2015) Bacterial and protist community changes during a phytoplankton bloom. Limnol Oceanogr 61:198–213. CrossRefGoogle Scholar
  17. 17.
    Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, Chow CET, Sachdeva R, Jones AC, Schwalbach MS, Rose JM, Hewson I, Patel A, Sun F, Caron DA, Fuhrman JA (2011) Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J 5:1414–1425. CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550. CrossRefPubMedGoogle Scholar
  19. 19.
    Shimaraev MN, Verbolov VI, Granin NG, Sherstayankin PP (1994) Physical limnology of Lake Baikal: a review. Baikal Intl. Cent. Ecol. Res, IrkutskGoogle Scholar
  20. 20.
    Popovskaya GI, Likhoshway YV, Genkal SI, Firsova AD (2006) The role of endemic diatom algae in the phytoplankton of Lake Baikal. Hydrobiologia 568:87–94. CrossRefGoogle Scholar
  21. 21.
    Annenkova NV (2013) Phylogenetic relations of the dinoflagellate Gymnodinium baicalense from Lake Baikal. Cent Eur J Biol 8:366–373. CrossRefGoogle Scholar
  22. 22.
    Belykh OI, Semenova EA, Kuznedelov KD, Zaika EI, Guselnikova NE (2000) A eukaryotic alga from picoplankton of Lake Baikal: morphology, ultrastructure and rDNA sequence data. Hydrobiologia 435:83–90. CrossRefGoogle Scholar
  23. 23.
    Fietz S, Bleib W, Hepperle D, Koppitz H, Krienitz L, Nicklisch A (2005) First record of Nannochloropsis limnetica (Eustigmatophyceae) in the autotrophic picoplankton from Lake Baikal. J Phycol 41:780–790. CrossRefGoogle Scholar
  24. 24.
    Obolkina LA (2006) Planktonic ciliates of Lake Baikal. Hydrobiologia 568:193–199. CrossRefGoogle Scholar
  25. 25.
    Yi Z, Berney C, Hartikainen H, Mahamdallie S, Gardner M, Boenigk J, Cavalier-Smith T, Bass D (2017) High throughput sequencing of microbial eukaryotes in Lake Baikal reveals ecologically differentiated communities and novel evolutionary radiations. FEMS Microbiol Ecol 93.
  26. 26.
    Parfenova VV, Gladkikh AS, Belykh OI (2013) Comparative analysis of biodiversity in the planktonic and biofilm bacterial communities in Lake Baikal. Microbiology 82:91–101. CrossRefGoogle Scholar
  27. 27.
    Zakharova YR, Galachyants YP, Kurilkina MI, Likhoshvay AV, Petrova DP, Shishlyannikov SM, Ravin NV, Mardanov AV, Beletsky AV, Likhoshway YV (2013) The structure of microbial community and degradation of diatoms in the deep near-bottom layer of Lake Baikal. PLoS One 8:e59977. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Bashenkhaeva MV, Zakharova YR, Petrova DP, Khanaev IV, Galachyants YP, Likhoshway YV (2015) Sub-ice microalgal and bacterial communities in freshwater Lake Baikal, Russia. Microb Ecol 70:751–765. CrossRefPubMedGoogle Scholar
  29. 29.
    Kurilkina MI, Zakharova YR, Galachyants YP, Petrova DP, Bukin YS, Domysheva VM, Blinov VV, Likhoshway EV (2016) Bacterial community composition in the water column of the deepest freshwater Lake Baikal as determined by next-generation sequencing. FEMS Microbiol Ecol 92.
  30. 30.
    Wetzel RG, Likens GE (1991) Limnological analyses. Springer-Verlag, New YorkCrossRefGoogle Scholar
  31. 31.
    Stroganov NS, Buzinova NS (1980) A practical guide to the hydrochemistry. Moscow University Press, MoscowGoogle Scholar
  32. 32.
    Boeva LV (2009) Manual for chemical analysis of land surface waters. NOK, Rostov-on-DonGoogle Scholar
  33. 33.
    Mikhailov IS, Zakharova YR, Galachyants YP, Usoltseva MV, Petrova DP, Sakirko MV, Likhoshway EV, Grachev MA (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. CrossRefPubMedGoogle Scholar
  34. 34.
    Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555. CrossRefPubMedGoogle Scholar
  35. 35.
    Nolte V, Pandey RV, Jost S, Medinger R, Ottenwälder B, Boenigk J, Schlӧtterer C (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol Ecol 19:2908–2915. CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    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 75:7537–7541. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:1–18. CrossRefGoogle Scholar
  38. 38.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Smith EP, van Belle G (1984) Nonparametric estimation of species richness. Biometrics 40:119–129CrossRefGoogle Scholar
  40. 40.
    Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542CrossRefGoogle Scholar
  41. 41.
    McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al (2016) vegan: Community Ecology Package. Version 2.4–1.
  43. 43.
    Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York CrossRefGoogle Scholar
  44. 44.
    Royston P (1995) Remark AS R94: a remark on algorithm AS 181: the W-test for normality. Appl Stat-J Roy St C 44:547–551Google Scholar
  45. 45.
    Hollander M, Wolfe DA (1973) Nonparametric statistical methods. Wiley, New YorkGoogle Scholar
  46. 46.
    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300Google Scholar
  47. 47.
    Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T et al (2015) gplots: various R programming tools for plotting data. R package version 2.17.0.
  48. 48.
    Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9Google Scholar
  49. 49.
    Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. CrossRefGoogle Scholar
  50. 50.
    Logue JB, Mouquet N, Peter H, Hillebrand H, The Metacommunity Working Group (2011) Empirical approaches to metacommunities: a review and comparison with theory. Trends Ecol Evol 26:482–491. CrossRefPubMedGoogle Scholar
  51. 51.
    Shimaraev MN, Granin NG (1991) Temperature stratification and the mechanism of convection in Lake Baikal. Dokl Akad Nauk 321:381–385Google Scholar
  52. 52.
    Weiss RF, Carmack EC, Koropalov VM (1991) Deep-water renewal and biological production in Lake Baikal. Nature 349:665–669CrossRefGoogle Scholar
  53. 53.
    Shimaraev MN, Granin NG, Domysheva VM, Zhdanov AA, Golobkova LP, Gnatovsky RY, Cehanovsky VV, Blinov VV (2003) Inter-basin water exchange in Lake Baikal. Vodniye resursi 30:678–681Google Scholar
  54. 54.
    Domysheva VM, Usoltseva MV, Sakirko MV, Pestunov DA, Shimaraev MN, Popovskaya GI, Panchenko MV (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. CrossRefGoogle Scholar
  55. 55.
    Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol R 75:14–49. CrossRefGoogle Scholar
  56. 56.
    Humbert JF, Dorigo U, Cecchi P, Le Berre B, Debroas D, Bouvy M (2009) Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ Microbiol 11:2339–2350. CrossRefPubMedGoogle Scholar
  57. 57.
    Glӧckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66:5053–5065CrossRefGoogle Scholar
  58. 58.
    Salcher MM, Pernthaler J, Posch T (2010) Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake. Limnol Oceanogr 55:846–856. CrossRefGoogle Scholar
  59. 59.
    Jezbera J, Horňak K, Šimek K (2006) Prey selectivity of bacterivorous protists in different size fractions of reservoir water amended with nutrients. Environ Microbiol 8:1330–1339. CrossRefPubMedGoogle Scholar
  60. 60.
    Williams TJ, Wilkins D, Long E, Evans F, DeMaere MZ, Raftery MJ, Cavicchioli R (2013) The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ Microbiol 15:1302–1317. CrossRefPubMedGoogle Scholar
  61. 61.
    Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100. CrossRefPubMedGoogle Scholar
  62. 62.
    Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatom and bacteria. Microbiol Mol Biol Rev 76:667–684. CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Urbach E, Vergin KL, Young L, Morse A, Larson GL, Giovannoni SJ (2001) Unusual bacterioplankton community structure in ultra-oligotrophic Crater Lake. Limnol Oceanogr 46:557–572. CrossRefGoogle Scholar
  64. 64.
    Urbach E, Vergin KL, Larson GL, Giovannoni SJ (2007) Bacterioplankton communities of Crater Lake, OR: dynamic changes with euphotic zone food web structure and stable deep water populations. Hydrobiologia 574:161–177. CrossRefGoogle Scholar
  65. 65.
    Obolkina LA, Potapskaya NV, Belykh OI, Pomazkina GI, Blinov VV, Zhdanov AA (2012) Seasonal dynamics of ciliates and microalgae in the pelagic zone of Southern Baikal. Hydrobiol J 48:11–19Google Scholar
  66. 66.
    Boenigk J, Arndt H (2002) Bacterivory by heterotrophic flagellates: community structure and feeding strategies. A van Leeuw J Microb 81:465–480. CrossRefGoogle Scholar
  67. 67.
    Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728. CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Lee SH, Ka JO, Cho JC (2008) Members of the phylum Acidobacteria are dominant and metabolically active in rhizosphere soil. FEMS Microbiol Lett 285:263–269. CrossRefPubMedGoogle Scholar
  69. 69.
    Quaiser A, Lopez-Garcia P, Zivanovic Y, Henn MR, Rodriguez-Valera F, Moreira D (2008) Comparative analysis of genome fragments of Acidobacteria from deep Mediterranean plankton. Environ Microbiol 10:2704–2717. CrossRefPubMedGoogle Scholar
  70. 70.
    Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19:926–936. CrossRefPubMedGoogle Scholar
  71. 71.
    Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. BioScience 46:609–620CrossRefGoogle Scholar
  72. 72.
    Vacher C, Tamaddoni-Nezhad A, Kamenova S, Peyrard N, Moalic Y, Sabbadin et al (2016) Chapter one-learning ecological networks from next-generation sequencing data. Adv Ecol Res 54:1–39CrossRefGoogle Scholar
  73. 73.
    Weiss S, Van Treuren W, Lozupone C, Faust K, Friedman J, Deng Y et al (2016) Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J 10:1669–1681. CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Zeder M, Peter S, Shabarova T, Pernthaler J (2009) A small population of planktonic Flavobacteria with disproportionally high growth during the spring phytoplankton bloom in a prealpine lake. Environ Microbiol 11:2676–2686. CrossRefPubMedGoogle Scholar
  75. 75.
    Ghylin TW, Garcia SL, Moya F, Oyserman BO, Schwientek P, Forest KT, Mutschler J, Dwulit-Smith J, Chan LK, Martinez-Garcia M, Sczyrba A, Stepanauskas R, Grossart HP, Woyke T, Warnecke F, Malmstrom R, Bertilsson S, McMahon KD (2014) Comparative single-cell genomics reveals potential ecological niches for the freshwater acl Actinobacteria lineage. ISME J 8:2503–2516. CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Jezbera J, Jezberova J, Koll U, Horňak K, Šimek K, Hahn MW (2012) Contrasting trends in distribution of four major planktonic betaproteobacterial groups along a pH gradient of epilimnia of 72 freshwater habitats. FEMS Microbiol Ecol 81:467–479. CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Šimek K, Jürgens K, Nedoma J, Comerma M, Armengol J (2000) Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat Microb Ecol 22:43–56. CrossRefGoogle Scholar
  78. 78.
    Comte J, Jacquet S, Vibound S, Fontvieille D, Millery A, Paolini G, Domaizon I (2006) Microbial community structure and dynamics in the largest natural French Lake (Lake Bourget). Microb Ecol 52:72–89. CrossRefPubMedGoogle Scholar
  79. 79.
    Popovskaya GI (2000) Ecological monitoring of phytoplankton in Lake Baikal. Aquat Ecosyst Health 3:215–225. CrossRefGoogle Scholar
  80. 80.
    Belykh OI, Sorokovikova EG (2003) Autotrophic picoplankton in Lake Baikal: abundance, dynamics, and distribution. Aquat Ecosyst Health 6:251–261. CrossRefGoogle Scholar
  81. 81.
    Wurzbacher CM, Bärlocher F, Grossart HP (2010) Fungi in lake ecosystems. Aquat Microb Ecol 59:125–149. CrossRefGoogle Scholar
  82. 82.
    Sime-Ngando T (2012) Phytoplankton chytridiomycosis: fungal parasites of phytoplankton and their imprints on the food web dynamics. Front Microbiol 3:1–13. CrossRefGoogle Scholar
  83. 83.
    Rasconi S, Niquil N, Sime-Ngando T (2012) Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic systems. Environ Microbiol 14:2151–2170. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Limnological InstituteSiberian Branch of the Russian Academy of SciencesIrkutskRussia

Personalised recommendations