Microbial Ecology

, Volume 76, Issue 2, pp 372–386 | Cite as

Taxonomical Resolution and Distribution of Bacterioplankton Along the Vertical Gradient Reveals Pronounced Spatiotemporal Patterns in Contrasted Temperate Freshwater Lakes

  • J. Keshri
  • A. S. Pradeep RamEmail author
  • P. A. Nana
  • T. Sime-Ngando
Environmental Microbiology


We examined the relationship between viruses and co-occurring bacterial communities across spatiotemporal scale in two contrasting freshwater lakes, namely meromictic Lake Pavin and dimictic Lake Aydat (Central France). Next-generation sequencing of 16S rRNA genes suggested distinct patterns in bacterioplankton community composition (BCC) between the lakes over depths and seasons. BCC were generally dominated by members of Actinobacteria, Proteobacteria, and Bacteroidetes covering about 95% of all sequences. Oxygen depletion at the bottom waters in Aydat and existence of permanent anoxia in the monimolimnion of Pavin resulted in the occurrence and dominance of lesser known members of lake communities such as Methylotenera, Methylobacter, Gallionella, Sulfurimonas, and Syntrophus in Pavin and Methylotenera and Sulfuritalea in Aydat. Differences in BCC appeared strongly related to dissolved oxygen concentration, temperature, viral infection, and virus-to-bacteria ratio. UniFrac analysis indicated a clear distinction in BCC when the percentage of viral infected bacterial cells and virus-to-bacteria ratio exceeded a threshold level of 10% and 5, respectively, suggesting a link between viruses and their potential bacterial host communities. Our study revealed that in both the lakes, the prevailing environmental factors across time and space structured and influenced the adaptation of bacterial communities to specific ecological niches.


Bacterial community composition and diversity Illumina sequencing Viral lysis Physicochemical gradients Temperate lakes Microbial ecology 



JK was supported by a postdoctoral fellowship from the Université Clermont-Auvergne (France). We thank J. Colombet and F. Perriere for their technical assistance in flow cytometry and nutrient analysis. We appreciate the two reviewers for their time, effort, and valuable contributions to this manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Supplementary material

248_2018_1143_MOESM1_ESM.docx (284 kb)
ESM 1 (DOCX 284 kb)


  1. 1.
    Cotner JB, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121CrossRefGoogle Scholar
  2. 2.
    Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791CrossRefPubMedGoogle Scholar
  3. 3.
    Salcher MM, Pernthaler J, Posch T (2010) Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake. Limnol. Oceanogr 55:846–856CrossRefGoogle Scholar
  4. 4.
    Garcia SL, Salka I, Grossart HP et al (2013) Depth-discrete profiles of bacterial communities reveal pronounced spatio-temporal dynamics related to lake stratification. Environ Microbiol Rep 5:549–555CrossRefPubMedGoogle Scholar
  5. 5.
    Comeau AM, Harding T, Galand PE et al (2012) Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Sci Rep 2:604CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Jones SE, Cadkin TA, Newton RJ et al (2012) Spatial and temporal scales of aquatic bacterial beta diversity. Front Microbiol 3:318CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Sandaa R-A, Gomez-Consarnau L, Pinhassi J et al (2009) Viral control of bacterial biodiversity-evidence from a nutrient enriched marine mesocosm experiment. Environ Microbiol 11:2585–2597CrossRefPubMedGoogle Scholar
  8. 8.
    Bouvy M, Bettarel Y, Bouvier C et al (2011) Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change. Environ Microbiol 13:1842–1857CrossRefPubMedGoogle Scholar
  9. 9.
    Berdjeb L, Ghiglione JF, Jacquet S (2011) Bottom-up versus top-down control of hypo- and epilimnion free-living bacterial community structures in two neighboring freshwater lakes. Appl Environ Microbiol 77:3591–3599CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Llirós M, Inceoğlu Ö, García-Armisen T et al (2014) Bacterial community composition in three freshwater reservoirs of different alkalinity and trophic status. PLoS One 9:e116145CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Schwalbach M, Hewson I, Fuhrman J (2004) Viral effects on bacterial community composition in marine plankton microcosms. Aquat Microb Ecol. 34:117–127CrossRefGoogle Scholar
  12. 12.
    Pradeep Ram AS, Chaibi-Slouma S, Keshri J et al (2016) Functional responses of bacterioplankton diversity and metabolism to experimental bottom-up and top-down forcings. Microb Ecol 72:347–358CrossRefPubMedGoogle Scholar
  13. 13.
    Suttle CA (2007) Viruses in the sea. Nature 437:356–361CrossRefGoogle Scholar
  14. 14.
    Sime-Ngando T (2014) Environmental bacteriophages: viruses of microbes in aquatic systems. Front Microbiol 5:1–14CrossRefGoogle Scholar
  15. 15.
    Bouvier T, del Giorgio PA (2007) Key role of selective viral-induced mortality in determining marine bacterial community composition. Environ. Microbiol. 9:287–297CrossRefPubMedGoogle Scholar
  16. 16.
    Pradeep Ram AS, Sime-Ngando T (2008) Functional responses of prokaryotes and viruses to grazer effects and nutrient additions in freshwater microcosms. ISME J 2:498–509CrossRefPubMedGoogle Scholar
  17. 17.
    Jardillier L, Boucher D, Personnic S et al (2005) Relative importance of nutrients and mortality factors on prokaryotic community composition in two lakes of different trophic status: microcosm experiments. FEMS Microb Ecol 53:429–443CrossRefGoogle Scholar
  18. 18.
    Zinger L, Gobet A, Pommiers T (2012) Two decades of describing the unseen majority of aquatic microbial diversity. Mol Ecol 21:1878–1896CrossRefPubMedGoogle Scholar
  19. 19.
    Liu L, Yang J, Yu Z et al (2015) The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J 9:2068–2077CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Hayden CJ, Beman JM (2016) Microbial diversity and community structure along a lake elevation gradient in Yosemite national park, California, USA. Environ Microbiol 18:1782–1791CrossRefPubMedGoogle Scholar
  21. 21.
    Bettarel Y, Sime-Ngando T, Amblard C, Dolan J (2004) Viral activity in two contrasting lake ecosystems. Appl Environ Microbiol 70:2941–2951CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Pradeep Ram AS, Rasconi S, Jobard M et al (2011) High lytic infection rates but low abundances of prokaryote viruses in a humic lake (Vassiviére, Massif Central, France). Appl Environ Microbiol 77:5610–5618CrossRefPubMedCentralGoogle Scholar
  23. 23.
    Wetzel RG, Likens GE (1995) Limnological analysis2nd edn. Springer-Verlag, New YorkGoogle Scholar
  24. 24.
    Lønborg C, Søndergaard M (2009) Microbial availability and degradation of dissolved organic carbon and nitrogen in two coastal areas. Estuar Coast Shelf Sci 81:513–520CrossRefGoogle Scholar
  25. 25.
    Mahaffey C, Benitez-Nelson CR, Bidigare RR et al (2008) Nitrogen dynamics within a wind-driven eddy. Deep Sea Res II 55:1398–1411CrossRefGoogle Scholar
  26. 26.
    Brussaard C, Payet JP, Winter C et al (2010) Quantification of aquatic viruses by flow cytometry. In: Wilhelm SW, Weinbauer MG, Suttle C (eds) Manual of aquatic viral ecology. American Society of Limnology and Oceanography, Texas, pp 102–109CrossRefGoogle Scholar
  27. 27.
    Weinbauer MG, Höfle MG (1998) Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl Environ Microbiol 64:431–438PubMedPubMedCentralGoogle Scholar
  28. 28.
    Weinbauer MG, Winter C, Höfle MG (2002) Reconsidering transmission electron microscopy based estimates of viral infection of bacterioplankton using conversion factors derived from natural communities. Aquat Microb Ecol 27:103–110CrossRefGoogle Scholar
  29. 29.
    Liu Z, Lozupone C, Hamady M et al (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Polz MF, Cavanaugh CM (1998) Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64:3724–3730PubMedPubMedCentralGoogle Scholar
  31. 31.
    Kennedy K, Hall MW, Lynch MD, Moreno-Hagelsieb G, Neufeld JD (2014) Evaluating bias of Illumina-based bacterial 16S rRNA gene profiles. Appl Environ Microbiol 80:5717–5722CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Pascault N, Roux S, Artigas J et al (2014) A high-throughput sequencing ecotoxicology study of freshwater bacterial communities and their responses to tebuconazole. FEMS Microb Ecol 90:563–574CrossRefGoogle Scholar
  33. 33.
    Li S, Bronner G, Lepère C, Kong F, Shi X (2017) Temporal and spatial variations in the composition of freshwater photosynthetic picoeukaryotes revealed by MiSeq sequencing from flow cytometry sorted samples. Environ Microbiol 19:2286–2300CrossRefPubMedGoogle Scholar
  34. 34.
    Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Pruesse E, Quast C, Knittel K et al (2007) SILVA, a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Yue JC, Clayton MK (2005) A similarity measure based on species proportions. Commun Stat – Theory Methods 34:2123–2131CrossRefGoogle Scholar
  40. 40.
    Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Avila MP, Staehr PA, Barbosa FAR et al (2017) Seasonality of freshwater bacterioplankton diversity in two tropical shallow lakes from the Brazilian Atlantic forest. FEMS Microb Ecol 93:218CrossRefGoogle Scholar
  42. 42.
    Ghai R, Mizuno CM, Picazo A et al (2014) Key roles for freshwater Actinobacteria revealed by deep metagenomics sequencing. Mol Ecol 23:6073–6090CrossRefPubMedGoogle Scholar
  43. 43.
    Allgaier M, Grossart HP (2006) Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany. Appl Environ Microbiol 72:3489–3497CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Glöckner FO, Zaichikov E, Belkova N et al (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Environ Microbiol 66:5053–5065CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Gomez-Consarnau L, Lindh MV, Gasol JM et al (2012) Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ Microbiol 14:2361–2378CrossRefPubMedGoogle Scholar
  46. 46.
    Tarao M, Jezbera J, Hahn MW (2009) Involvement of cell surface structures in size-independent grazing resistance of freshwater Actinobacteria. Appl Environ Microbiol 75:4720–4726CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Mustakhimov I, Kalyuzhnaya MG, Lidstrom MW et al (2013) Insights into denitrification in Methylotenera mobilis from denitrification pathway and methanol metabolism mutants. J Bacteriol 195:2207–2211CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Hernandez ME, Beck DAC, Lidstrom ME et al (2015) Oxygen availability is a major factor in determining the composition of microbial communities involved in methane oxidation. Peer J 3:e801CrossRefPubMedGoogle Scholar
  49. 49.
    Grote J, Schott T, Bruckner CG et al (2012) Genome and physiology of a model Epsilonproteobacterium responsible for sulphide detoxification in marine oxygen depletion zones. Proc Natl Acad Sci U S A 109:506–510CrossRefPubMedGoogle Scholar
  50. 50.
    Biderre-Petit C, Jézéquel D, Dugat-Bony E et al (2011) Identification of microbial communities involved in the methane cycle of a freshwater meromictic lake. FEMS Microb Ecol 77:533–545CrossRefGoogle Scholar
  51. 51.
    Tiodjio RE, Sakatoku A, Nakamura A et al (2014) Bacterial and archaeal communities in Lake Nyos (Cameroon, Central Africa). Sci Rep 4:6151CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Kim C, Nishimura Y, Nagata T (2003) Role of dissolved organic matter in the hypolimnetic mineralization of carbon and nitrogen in a large monomictic lake. Limnol Oceanogr 51:70–78CrossRefGoogle Scholar
  53. 53.
    Barberán A, Casamayor EO (2010) Global phylogenetic community structure and β-diversity patterns in surface bacterioplankton metacommunities. Aquat Microb Ecol 59:1–10CrossRefGoogle Scholar
  54. 54.
    Auguet JC, Montanié H, Hartmann HJ, Lebaron P, Casamayor EO, Catala P, Delmas D (2009) Potential effect of freshwater virus on the structure and activity of bacterial communities in the Marennes-Oleron Bay (France). Microb Ecol 57:295–306CrossRefPubMedGoogle Scholar
  55. 55.
    Storesund JE, Erga SR, Ray JL et al (2015) Top-down and bottom-up control on bacterial diversity in a western Norwegian deep-silled fjord. FEMS Microb Ecol 91:7CrossRefGoogle Scholar
  56. 56.
    Thingstad T, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19–27CrossRefGoogle Scholar
  57. 57.
    Montanié H, De Crignis MG, Lavaud J (2015) Viral impact on prokaryotic and microalgal activities in the microphytobenthic biofilm of an intertidal mudflat (French Atlantic Coast). Front Microbiol 6:1214CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Pradeep Ram AS, Colombet J, Perriere F, Thouvenot A, Sime-Ngando T (2016) Viral regulation of prokaryotic carbon metabolism in a hypereutrophic freshwater reservoir ecosystem (Villerest, France). Front Microbiol 7:81CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Pradeep Ram AS, Colombet J, Perriere F, Thouvenot A, Sime-Ngando T (2015) Viral and grazer regulation of prokaryotic growth efficiency in temperate freshwater pelagic environments. FEMS Microbiol Ecol 91:1–12CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  • J. Keshri
    • 1
    • 2
  • A. S. Pradeep Ram
    • 1
    Email author
  • P. A. Nana
    • 1
  • T. Sime-Ngando
    • 1
  1. 1.Laboratoire Microorganismes: Génome et Environnement, UMR CNRS 6023Université Clermont-AuvergneAubière CedexFrance
  2. 2.Institute of Postharvest and Food SciencesAgricultural Research OrganizationBet DaganIsrael

Personalised recommendations