Skip to main content
SpringerLink
Log in

Effect of Nutrient Loading on Bacterioplankton Community Composition in Lake Mesocosms

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Changes in bacterioplankton community composition were followed in mesocosms set up in the littoral of Lake Vesijärvi, southern Finland, over two summers. Increasing nitrogen and phosphorus concentrations in the mesocosms represented different trophic states, from mesotrophic to hypertrophic. In 1998, the mesocosms were in a turbid state with a high biomass of phytoplankton, whereas in 1999, macrophytes proliferated and a clear-water state prevailed. The bacterial communities in the mesocosms also developed differently, as shown by denaturing gradient gel electrophoresis profiling of partial 16S rRNA gene fragments and by nonmetric multidimensional scaling analysis. In 1998, nutrient treatments affected the diversity and clustering of bacterial communities strongly, but in 1999, the bacterial communities were less diversified and not clearly affected by treatments. Canonical correspondence analysis indicated that bacterioplankton communities in the mesocosms were influenced by environmental physicochemical variables linked to the increasing level of eutrophication. Nitrogen concentration correlated directly with the bacterioplankton composition. In addition, the high nutrient levels had indirect effects through changes in the biomass and composition of phyto- and zooplankton. Sequencing analysis showed that the dominant bacterial divisions remained the same, but the dominant phylotypes changed during the 2-year period. The occurrence of Verrucomicrobia correlated with more eutrophic conditions, whereas the occurrence of Actinobacteria correlated with less eutrophic conditions.

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

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. RI Amann W Ludwig KH Schleifer (1995) ArticleTitlePhylogenetic identification and in situ detection of individual microbial cells without cultivation Microbiol Rev 59 143–169 Occurrence Handle1:CAS:528:DyaK2MXkvVGmurk%3D Occurrence Handle7535888

    CAS  PubMed  Google Scholar 

  2. TR Anderson DO Hessen JJ Elser J Urabe (2005) ArticleTitleMetabolic stoichiometry and the fate of excess carbon and nutrients in consumers Am Nat 165 1–15 Occurrence Handle10.1086/426598 Occurrence Handle15729636

    Article  PubMed  Google Scholar 

  3. CA Carlson SJ Giovannoni DA Hansell SJ Goldberg R Parsons MP Otero K Vergin BR Wheeler (2002) ArticleTitleEffect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea Aquat Microb Ecol 30 19–36

    Google Scholar 

  4. JB Cotner BA Biddanda (2002) ArticleTitleSmall players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems Ecosystems 5 105–121 Occurrence Handle10.1007/s10021-001-0059-3 Occurrence Handle1:CAS:528:DC%2BD38XjtlCnur4%3D

    Article  CAS  Google Scholar 

  5. BC Crump GW Kling M Bahr JE Hobbie (2003) ArticleTitleBacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source Appl Environ Microbiol 69 2253–2268 Occurrence Handle10.1128/AEM.69.4.2253-2268.2003 Occurrence Handle12676708

    Article  PubMed  Google Scholar 

  6. A Eiler S Bertilsson (2004) ArticleTitleComposition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes Environ Microbiol 6 1228–1243 Occurrence Handle10.1111/j.1462-2920.2004.00657.x Occurrence Handle15560821

    Article  PubMed  Google Scholar 

  7. LB Fandino L Riemann GF Steward RA Long F Azam (2001) ArticleTitleVariations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing Aquat Microb Ecol 23 119–130

    Google Scholar 

  8. MM Fisher JL Klug G Lauster M Newton EW Triplett (2000) ArticleTitleEffect of resources and trophic interactions on freshwater bacterioplankton diversity Microb Ecol 40 125–138 Occurrence Handle1:CAS:528:DC%2BD3cXotFCqs7w%3D Occurrence Handle11029081

    CAS  PubMed  Google Scholar 

  9. FO Glöckner E Zaichikov N Belkova L Denissova J Pernthaler A Pernthaler R Amann (2000) ArticleTitleComparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria Appl Environ Microbiol 66 5053–5065 Occurrence Handle11055963

    PubMed  Google Scholar 

  10. K Haukka E Heikkinen T Kairesalo H Karjalainen K Sivonen (2005) ArticleTitleEffect of humic material on the bacterioplankton community composition in boreal lakes and mesocosms Environ Microbiol 7 620–630 Occurrence Handle10.1111/j.1462-2920.2005.00724.x Occurrence Handle1:CAS:528:DC%2BD2MXksFCgsL4%3D Occurrence Handle15819844

    Article  CAS  PubMed  Google Scholar 

  11. J Hietala K Vakkilainen T Kairesalo (2004) ArticleTitleCommunity resistance and change to nutrient enrichment and fish manipulation in a vegetated lake littoral Freshw Biol 49 1525–1537 Occurrence Handle10.1111/j.1365-2427.2004.01303.x Occurrence Handle1:CAS:528:DC%2BD2MXhvV2itQ%3D%3D

    Article  CAS  Google Scholar 

  12. MG Höfle H Haas K Dominik (1999) ArticleTitleSeasonal dynamics of bacterioplankton community structure in a eutrophic lake as determined by 5S rRNA analysis Appl Environ Microbiol 65 3164–3174 Occurrence Handle10388718

    PubMed  Google Scholar 

  13. E Jeppesen TL Lauridsen T Kairesalo MR Perrow (1998) Impact of submerged macrophytes on fish–zooplankton interactions in lakes E Jeppesen M Søndergaard M Søndergaard K Christoffersen (Eds) The Structuring Role of Submerged Macrophytes in Lakes Springer Berlin 91–114

    Google Scholar 

  14. K Jürgens C Matz (2002) ArticleTitlePredation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria Antonie van Leeuwenhoek 81 413–434 Occurrence Handle10.1023/A:1020505204959 Occurrence Handle12448740

    Article  PubMed  Google Scholar 

  15. K Jürgens J Pernthaler S Schalla R Amann (1999) ArticleTitleMorphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing Appl Environ Microbiol 65 1241–1250 Occurrence Handle10049890

    PubMed  Google Scholar 

  16. E Kolmonen K Sivonen J Rapala K Haukka (2004) ArticleTitleDiversity of cyanobacteria and heterotrophic bacteria in cyanobacterial blooms in Lake Joutikas, Finland Aquat Microb Ecol 36 201–211

    Google Scholar 

  17. J Koski-Vähälä H Hartikainen P Tallberg (2001) ArticleTitlePhosphorus mobilization from various sediment pools in response to increased pH and silicate concentration J Environ Qual 30 546–552 Occurrence Handle11285916

    PubMed  Google Scholar 

  18. S Langenheder V Kisand J Wikner LJ Tranvik (2003) ArticleTitleSalinity as a structuring factor for the composition and performance of bacterioplankton degrading riverine DOC FEMS Microb Ecol 45 189–202 Occurrence Handle1:CAS:528:DC%2BD3sXlsVaisr4%3D

    CAS  Google Scholar 

  19. P Lebaron P Servais M Troussellier C Courties G Muyzer L Bernard H Schäfer R Pukall E Stackebrandt T Guindulain J Vives-Rego (2001) ArticleTitleMicrobial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in abundances, activity and composition FEMS Microbiol Ecol 34 255–266 Occurrence Handle1:CAS:528:DC%2BD3MXht1Ghuro%3D Occurrence Handle11137605

    CAS  PubMed  Google Scholar 

  20. ES Lindström (2000) ArticleTitleBacterioplankton community composition in five lakes differing in trophic status and humic content Microb Ecol 40 104–113 Occurrence Handle11029079

    PubMed  Google Scholar 

  21. ES Lindström (2001) ArticleTitleInvestigating influential factors on bacterioplankton community composition: results from a field study of five mesotrophic lakes Microb Ecol 42 598–605 Occurrence Handle12024242

    PubMed  Google Scholar 

  22. ES Lindström K Vrede E Leskinen (2004) ArticleTitleResponse of a member of the Verrucomicrobia, among the dominating bacteria in a hypolimnion, to increased phosphorus availability J Plankton Res 26 241–246

    Google Scholar 

  23. A Lyche T Andersen K Christoffersen DO Hessen PHB Hansen A Klysner (1996) ArticleTitleMesocosm tracer studies. 2. The fate of primary production and the role of consumers in the pelagic carbon cycle of a mesotrophic lake Limnol Oceanogr 41 475–487 Occurrence Handle1:CAS:528:DyaK28XkvFKht7g%3D

    CAS  Google Scholar 

  24. K Muylaert K Gucht ParticleVan der N Vloemans L Meester ParticleDe M Gillis W Vyverman (2002) ArticleTitleRelationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes Appl Environ Microbiol 68 4740–4750 Occurrence Handle10.1128/AEM.68.10.4740-4750.2002 Occurrence Handle1:CAS:528:DC%2BD38XnvFClt70%3D Occurrence Handle12324315

    Article  CAS  PubMed  Google Scholar 

  25. G Muyzer K Smalla (1998) ArticleTitleApplication of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology Antonie van Leeuwenhoek 73 127–141 Occurrence Handle10.1023/A:1000669317571 Occurrence Handle1:CAS:528:DyaK1cXjsVaqtbs%3D Occurrence Handle9602286

    Article  CAS  PubMed  Google Scholar 

  26. A Ojala S Kokkonen T Kairesalo (2003) ArticleTitleThe role of phosphorus in growth of phytoplankton in Lake Vesijärvi, southern Finland—amultitechnique approach Aquat Sci 65 287–296 Occurrence Handle1:CAS:528:DC%2BD3sXovFWns7o%3D

    CAS  Google Scholar 

  27. L Øvreås D Bourne RA Sandaa EO Casamayor S Benlloch V Goddard G Smerdon M Heldal TF Thingstad (2003) ArticleTitleResponse of bacterial and viral communities to nutrient manipulations in seawater mesocosms Aquat Microb Ecol 31 109–121

    Google Scholar 

  28. J Pinhassi MM Sala H Havskum F Peters Ò Guadayol A Malits C Marrasé (2004) ArticleTitleChanges in bacterioplankton composition under different phytoplankton regimens Appl Environ Microbiol 70 6753–6766 Occurrence Handle10.1128/AEM.70.11.6753-6766.2004 Occurrence Handle1:CAS:528:DC%2BD2cXhtVSju73P Occurrence Handle15528542

    Article  CAS  PubMed  Google Scholar 

  29. R Pourriot (1977) ArticleTitleFood and feeding habits of Rotifera Arch Hydrobiol Beih Ergeb Limnol 8 243–260

    Google Scholar 

  30. A Puddu A Zoppini S Fazi M Rosati S Amalfitano E Magaletti (2003) ArticleTitleBacterial uptake of DOM released from P-limited phytoplankton FEMS Microb Ecol 46 257–268 Occurrence Handle1:CAS:528:DC%2BD3sXptlOru7g%3D

    CAS  Google Scholar 

  31. L Riemann GF Steward F Azam (2000) ArticleTitleDynamics of bacterial community composition and activity during a mesocosm diatom bloom Appl Environ Microbiol 66 578–587 Occurrence Handle1:CAS:528:DC%2BD3cXhtFeru7o%3D Occurrence Handle10653721

    CAS  PubMed  Google Scholar 

  32. L Riemann A Winding (2001) ArticleTitleCommunity dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom Microb Ecol 42 274–285 Occurrence Handle10.1007/s00248-001-0018-8 Occurrence Handle1:CAS:528:DC%2BD38XksFM%3D Occurrence Handle12024253

    Article  CAS  PubMed  Google Scholar 

  33. H Schäfer L Bernard C Courties P Lebaron P Servais R Pukall E Stackebrandt M Troussellier T Guindulain J Vives-Rego G Muyzer (2001) ArticleTitleMicrobial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations FEMS Microbiol Ecol 34 243–253 Occurrence Handle11137604

    PubMed  Google Scholar 

  34. M Scheffer SH Hosper ML Meijer B Moss E Jeppesen (1993) ArticleTitleAlternative equilibria in shallow lakes TREE 8 275–279

    Google Scholar 

  35. H Sekiguchi M Watanabe T Nakahara B Xu H Uchiyama (2002) ArticleTitleSuccession of bacterial community structure along the Changjiang River by denaturing gradient gel electrophoresis and clone library analysis Appl Environ Microbiol 68 5142–5150 Occurrence Handle10.1128/AEM.68.10.5142-5150.2002 Occurrence Handle1:CAS:528:DC%2BD38XnvFCksr0%3D Occurrence Handle12324365

    Article  CAS  PubMed  Google Scholar 

  36. M Søndergaard (1997) Bacteria and dissolved organic carbon in lakes K Sand-Jensen O Pedersen (Eds) Freshwater Biology G.E.C. Gad Publishers Copenhagen, Denmark 138–161

    Google Scholar 

  37. R Stepanauskas MA Moran BA Bergamaschi JT Hollibaugh (2003) ArticleTitleCovariance of bacterioplankton composition and environmental variables in a temperate delta system Aquat Microb Ecol 31 85–98

    Google Scholar 

  38. D Stephen DM Balayla E Bécares SE Collings C Fernández-Aláez M Fernández-Aláez C Ferriol P García J Gomá M Gyllström LA Hansson J Hietala T Kairesalo MR Miracle S Romo J Rueda A Ståhl-Delbanco M Svensson K Vakkilainen M Valentín WJ Bund ParticleVan de E Donk ParticleVan E Vicente MJ Villena B Moss (2004) ArticleTitleContinental-scale patterns of nutrient and fish effects on shallow lakes: introduction to a pan-European mesocosm experiment Freshw Biol 49 1517–1524 Occurrence Handle1:CAS:528:DC%2BD2MXhvV2itA%3D%3D

    CAS  Google Scholar 

  39. M Suzuki SJ Giovannoni (1996) ArticleTitleBias caused by template annealing in the amplification of 16S rRNA genes by PCR Appl Environ Microbiol 62 625–630 Occurrence Handle1:CAS:528:DyaK28XovVCrug%3D%3D Occurrence Handle8593063

    CAS  PubMed  Google Scholar 

  40. CJF Braak ParticleTer P Smilauer (2002) CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (version 4.5) Microcomputer Power Ithaca, NY, USA

    Google Scholar 

  41. K Gucht ParticleVan der K Sabbe L Meester ParticleDe N Vloemans G Zwart M Gillis W Vyverman (2001) ArticleTitleContrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes Environ Microbiol 3 680–690

    Google Scholar 

  42. EJ Hannen ParticleVan W Mooij MP Agterveld Particlevan HJ Gons HJ Laanbroek (1999) ArticleTitleDetritus-dependent development of the microbial community in an experimental system: qualitative analysis by denaturing gradient gel electrophoresis Appl Environ Microbiol 65 2478–2484 Occurrence Handle10347030

    PubMed  Google Scholar 

  43. DM Ward R Weller MM Bateson (1990) ArticleTitle16S rRNA sequences reveal numerous uncultured microorganisms in a natural community Nature 345 63–65 Occurrence Handle10.1038/345063a0 Occurrence Handle1:CAS:528:DyaK3cXktlOltbo%3D Occurrence Handle1691827

    Article  CAS  PubMed  Google Scholar 

  44. F Warnecke R Amann J Pernthaler (2004) ArticleTitleActinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages Environ Microbiol 6 242–253 Occurrence Handle10.1111/j.1462-2920.2004.00561.x Occurrence Handle1:CAS:528:DC%2BD2cXitlOhtbc%3D Occurrence Handle14871208

    Article  CAS  PubMed  Google Scholar 

  45. RG Wetzel (1983) Limnology EditionNumber2 Saunders Collage Pub New York

    Google Scholar 

  46. RG Wetzel M Søndergaard (1998) Role of submerged macrophytes for the microbial community and dynamics of dissolved organic carbon in aquatic ecosystems E Jeppesen M Søndergaard M Søndergaard K Christoffersen (Eds) The Structuring Role ofSubmerged Macrophytes in Lakes Springer Berlin 133–147

    Google Scholar 

  47. AC Yannarell EW Triplett (2005) ArticleTitleGeographic and environmental sources of variation in lake bacterial community composition Appl Environ Microbiol 71 227–239 Occurrence Handle10.1128/AEM.71.1.227-239.2005 Occurrence Handle1:CAS:528:DC%2BD2MXotlaqtQ%3D%3D Occurrence Handle15640192

    Article  CAS  PubMed  Google Scholar 

  48. E Zöllner B Santer M Boersma HG Hoppe K Jürgens (2003) ArticleTitleCascading predation effects of Daphnia and copepods on microbial food web components Freshw Biol 48 2174–2193

    Google Scholar 

  49. G Zwart BC Crump MP Kamst-van Agterveld F Hagen S Han (2002) ArticleTitleTypical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers Aquat Microb Ecol 28 141–155

    Google Scholar 

  50. G Zwart R Huismans MP Agterveld Particlevan Y Peer ParticleVan de P Rijk ParticleDe H Eenhoorn G Muyzer EJ Hannen Particlevan HJ Gons HJ Laanbroek (1998) ArticleTitleDivergent members of the bacterial division Verrucomicrobiales in a temperate freshwater lake FEMS Microbiol Ecol 25 159–169 Occurrence Handle1:CAS:528:DyaK1cXht1Wgsbo%3D

    CAS  Google Scholar 

  51. W Zwisler N Selje M Simon (2003) ArticleTitleSeasonal patterns of the bacterioplankton community composition in a large mesotrophic lake Aquat Microb Ecol 31 211–225

    Google Scholar 

Download references

Acknowledgments

We thank Totte Niittylä and Jaana Vaitomaa for technical assistance. Financial support for the study was received from the Academy of Finland (grants 395901 and 201576 to K.S. and grant 48827 to K.H.) and from the Maj and Tor Nessling Foundation to K.H. The mesocosm experiment was funded by the European Commission (grant ENV4-CT97-0420 to T.K.).

Author information

Author notes

  1. Kaisa Haukka

    Present address: National Public Health Institute, Mannerheimintie 166, 00300, Helsinki, Finland

Authors and Affiliations

  1. Department of Applied Chemistry and Microbiology, University of Helsinki, P.O. Box 56, Viikki Biocenter, 00014, Helsinki, Finland

    Kaisa Haukka, Eija Kolmonen, Rafiqul Hyder & Kaarina Sivonen

  2. Department of Ecological and Environmental Sciences, University of Helsinki, Niemenkatu 73, 15140, Lahti, Finland

    Jaana Hietala, Kirsi Vakkilainen & Timo Kairesalo

  3. Department of Mathematics, University of Helsinki, P.O. Box 4, 00014, Helsinki, Finland

    Heikki Haario

Authors
  1. Kaisa Haukka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eija Kolmonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafiqul Hyder
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jaana Hietala
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kirsi Vakkilainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Timo Kairesalo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Heikki Haario
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kaarina Sivonen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kaisa Haukka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haukka, K., Kolmonen, E., Hyder, R. et al. Effect of Nutrient Loading on Bacterioplankton Community Composition in Lake Mesocosms. Microb Ecol 51, 137–146 (2006). https://doi.org/10.1007/s00248-005-0049-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-005-0049-7

Keywords

Search

Navigation