Skip to main content

Advertisement

Log in

Annual Patterns in Bacterioplankton Community Variability in a Humic Lake

  • Microbial Observatories
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Bacterioplankton community composition (BCC) was monitored in a shallow humic lake in northern Wisconsin, USA, over 3 years using automated ribosomal intergenic spacer analysis (ARISA). Comparison of ARISA profiles of bacterial communities over time indicated that BCC was highly variable on a seasonal and annual scale. Nonmetric multidimensional scaling (MDS) analysis indicated little similarity in BCC from year to year. Nevertheless, annual patterns in bacterioplankton community diversity were observed. Trends in bacterioplankton community diversity were correlated to annual patterns in community succession observed for phytoplankton and zooplankton populations, consistent with the notion that food web interactions affect bacterioplankton community structure in this humic lake. Bacterioplankton communities experience a dramatic drop in richness and abundance each year in early summer, concurrent with an increase in the abundance of both mixotrophic and heterotrophic flagellates. A second drop in richness, but not abundance, is observed each year in late summer, coinciding with an intense bloom of the nonphagotrophic dinoflagellate Peridinium limbatum. A relationship between bacterial community composition, size, and abundance and the population dynamics of Daphnia was also observed. The noted synchrony between these major population and species shifts suggests that linkages across trophic levels play a role in determining the annual time course of events for the microbial and metazoan components of the plankton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. R Adrian B Schneider-Olt (1999) ArticleTitleTop-down effects of crustacean zooplankton on pelagic microorganisms in a mesotrophic lake. J Plankton Res 21 2175–2190 Occurrence Handle10.1093/plankt/21.11.2175

    Article  Google Scholar 

  2. J Arrieta G Herndl (2002) ArticleTitleChanges in bacterial β-glucosidase diversity during a coastal phytoplankton bloom. Limnol Oceanogr 47 594–599 Occurrence Handle1:CAS:528:DC%2BD38XjtFSgs78%3D

    CAS  Google Scholar 

  3. L Arvola K Salonen (2001) ArticleTitlePlankton community of a polyhumic lake with and without Daphnia longispina (Cladocera). Hydrobiologia 445 141–150 Occurrence Handle10.1023/A:1017588913646

    Article  Google Scholar 

  4. L Arvola T Tulonen (1998) ArticleTitleEffects of allochthonous dissolved organic matter and inorganic nutrients on the growth of bacteria and algae from a highly humic lake. Environ Int 24 509–520 Occurrence Handle1:CAS:528:DyaK1cXkvVSns7w%3D

    CAS  Google Scholar 

  5. D Bird J Kalff (1986) ArticleTitleBacterial grazing by planktonic lake algae. Science 231 493–495

    Google Scholar 

  6. DF Bird J Kalff (1987) ArticleTitleAlgal phagotrophy—regulating factors and importance relative to photosynthesis in Dinobryon (Chrysophyceae). Limnol Oceanogr 32 277–284 Occurrence Handle1:CAS:528:DyaL2sXktVCls78%3D

    CAS  Google Scholar 

  7. CW Burns M Schallenberg (1998) ArticleTitleImpacts of nutrients and zooplankton on the microbial food web of an ultra-oligotrophic lake. J Plankton Res 20 1501–1525

    Google Scholar 

  8. CW Burns M Schallenberg (2001) ArticleTitleShort-term impacts of nutrients, Daphnia, and copepods on microbial food-webs of an oligotrophic and eutrophic lake. N Z J Mar Freshwat Res 35 695–710

    Google Scholar 

  9. C Callieri R Bertoni G Corno (2002) ArticleTitleDynamics of bacteria and mixotrophic flagellates in an Alpine lake in relation to Daphnia population development. J Limnol 61 177–182

    Google Scholar 

  10. TH Chrzanowski K Simek (1993) ArticleTitleBacterial-growth and losses due to bacterivory in a mesotrophic lake. J Plankton Res 15 771–785

    Google Scholar 

  11. KR Clarke (1993) ArticleTitleNon-parametric multivariate analyses of changes in community structure. Aust J Ecol 18 117–143

    Google Scholar 

  12. KR Clarke RH Green (1988) ArticleTitleStatistical design and analysis for a “biological effects” study. Mar Ecol Prog Ser 46 213–226

    Google Scholar 

  13. JJ Cole (1999) ArticleTitleAquatic microbiology for ecosystem scientists: new and recycled paradigms in ecological microbiology. Ecosystems 2 215–225 Occurrence Handle10.1007/s100219900069

    Article  Google Scholar 

  14. 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 

  15. 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 

  16. H Degans E Zollner K Van der Gucht L De Meester K Jurgens (2002) ArticleTitleRapid Daphnia-mediated changes in microbial community structure: an experimental study. FEMS Microbiol Ecol 42 137–149

    Google Scholar 

  17. I Domaizon S Viboud D Fontvieille (2003) ArticleTitleTaxon-specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy—importance of mixotrophy. FEMS Microbiol Ecol 46 317–329

    Google Scholar 

  18. 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 

  19. MM Fisher JM Graham LE Graham (1998) ArticleTitleBacterial abundance and activity across sites within two northern Wisconsin Sphagnum bogs. Microb Ecol 36 259–269 Occurrence Handle10.1007/s002489900113 Occurrence Handle9852506

    Article  PubMed  Google Scholar 

  20. MM Fisher JL Klug G Lauster M Newton EW Triplett (2000) ArticleTitleEffects 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 

  21. MM Fisher EW Triplett (1999) ArticleTitleAutomated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65 4630–4636

    Google Scholar 

  22. JM Gasol D Vaque (1993) ArticleTitleLack of coupling between heterotrophic nanoflagellates and bacteria—a general phenomenon across aquatic systems. Limnol Oceanogr 38 657–665

    Google Scholar 

  23. PM Glibert (1998) ArticleTitleInteractions of top-down and bottom-up control in planktonic nitrogen cycling. Hydrobiologia 363 1–12

    Google Scholar 

  24. JM Graham AD Kent GH Lauster AC Yannarell LE Graham TK Kratz EW Triplett (2003) ArticleTitleSeasonal dynamics of phytoplankton and protoplankton communities in a northern temperate humic lake: diversity in a dinoflagellate dominated system. Microb Ecol 48(4) in press

    Google Scholar 

  25. JP Grover (2000) ArticleTitleResource competition and community structure in aquatic microorganisms: experimental studies of algae and bacteria along a gradient of organic carbon to inorganic phosphorus supply. J Plankton Res 22 1591–1610 Occurrence Handle10.1093/plankt/22.8.1591 Occurrence Handle1:CAS:528:DC%2BD3cXmtlCksrY%3D

    Article  CAS  Google Scholar 

  26. MW Hahn MG Höfle (1999) ArticleTitleFlagellate predation on a bacterial model community: interplay of size-selective grazing, specific bacterial cell size, and bacterial community composition. Appl Environ Microbiol 65 4863–4872

    Google Scholar 

  27. MW Hahn MG Höfle (2001) ArticleTitleGrazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35 113–121

    Google Scholar 

  28. H Hillebrand CD Durselen D Kirschtel U Pollingher T Zohary (1999) ArticleTitleBiovolume calculation for pelagic and benthic microalgae. J Phycol 35 403–424 Occurrence Handle10.1046/j.1529-8817.1999.3520403.x

    Article  Google Scholar 

  29. RB Hitchman HLJ Jones (2000) ArticleTitleThe role of mixotrophic protists in the population dynamics of the microbial food web in a small artificial pond. Freshwat Biol 43 231–241 Occurrence Handle10.1046/j.1365-2427.2000.00541.x

    Article  Google Scholar 

  30. 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

    Google Scholar 

  31. A Isaksson AK Bergstrom P Blomqvist M Jansson (1999) ArticleTitleBacterial grazing by phagotrophic phytoflagellates in a deep humic lake in northern Sweden. J Plankton Res 21 247–268 Occurrence Handle10.1093/plankt/21.2.247

    Article  Google Scholar 

  32. E Jeppesen M Erlandsen M Sondergaard (1997) ArticleTitleCan simple empirical equations describe the seasonal dynamics of bacterioplankton in lakes: an eight-year study in shallow hypertrophic and biologically highly dynamic Lake Sobygard, Denmark. Microb Ecol 34 11–26 Occurrence Handle10.1007/s002489900030 Occurrence Handle9178602

    Article  PubMed  Google Scholar 

  33. RI Jones S Rees (1994) ArticleTitleInfluence of temperature and light on particle ingestion by the freshwater phytoflagellate Dinobryon. Archiv für Hydrobiologie 132 203–211

    Google Scholar 

  34. K Jurgens H Gude (1994) ArticleTitleThe potential importance of grazing-resistant bacteria in planktonic systems. Mar Ecol Prog Ser 112 169–188

    Google Scholar 

  35. K Jurgens E Jeppesen (2000) ArticleTitleThe impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. J Plankton Res 22 1047–1070 Occurrence Handle10.1093/plankt/22.6.1047

    Article  Google Scholar 

  36. K Jurgens MM Sala (2000) ArticleTitlePredation-mediated shifts in size distribution of microbial biomass and activity during detritus decomposition. Oikos 91 29–40

    Google Scholar 

  37. K Kato (1996) ArticleTitleBacteria—a link among ecosystem constituents. Res Popul Ecol 38 185–190

    Google Scholar 

  38. AP Kinzig SW Pacala (Eds) (2001) The Functional Consequences of Biodiversity: Empirical Progress and Theoretical Extensions Princeton University Press Princeton, NJ

    Google Scholar 

  39. W Lampert (1978) ArticleTitleRelease of dissolved organic carbon by zooplankton grazing. Limnol Oceanogr 23 831–843 Occurrence Handle1:CAS:528:DyaE1cXlsVelt7k%3D

    CAS  Google Scholar 

  40. S Langenheder K Jurgens (2001) ArticleTitleRegulation of bacterial biomass and community structure by metazoan and protozoan predation. Limnol Oceanogr 46 121–134

    Google Scholar 

  41. P Lebaron P Servais M Troussellier C Courties G Muyzer L Bernard H Schafer 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 Handle10.1016/S0168-6496(00)00103-3 Occurrence Handle1:CAS:528:DC%2BD3MXht1Ghuro%3D Occurrence Handle11137605

    Article  CAS  PubMed  Google Scholar 

  42. P Lebaron P Servais M Troussellier C Courties J Vives-Rego G Muyzer L Bernard T Guindulain H Schafer E Stackebrandt (1999) ArticleTitleChanges in bacterial community structure in seawater mesocosms differing in their nutrient status. Aquat Microb Ecol 19 255–267

    Google Scholar 

  43. ES Lindstrom (2000) ArticleTitleBacterioplankton community composition in five lakes differing in trophic status and humic content. Microb Ecol 40 104–113 Occurrence Handle1:CAS:528:DC%2BD3cXotFCqs78%3D Occurrence Handle11029079

    CAS  PubMed  Google Scholar 

  44. ES Lindstrom (2001) ArticleTitleInvestigating influential factors on bacterioplankton community composition: results from a field study of five mesotrophic lakes. Microb Ecol 42 598–605 Occurrence Handle10.1007/s00248-001-0031-y Occurrence Handle1:CAS:528:DC%2BD38XntFajsA%3D%3D Occurrence Handle12024242

    Article  CAS  PubMed  Google Scholar 

  45. JJ Magnuson TK Kratz TF Allen DE Armstrong BJ Benson CJ Bowser DW Bolgrien SR Carpenter TF Frost ST Gower TM Lillesand JA Pike MG Turner (1997) ArticleTitleRegionalization of long-term ecological research (LTER) on north temperate lakes. Verh Internal Verein Limnol 26 522–528

    Google Scholar 

  46. AE Magurran (1988) Ecological Diversity and Its Measurement Princeton University Press Princeton, NJ

    Google Scholar 

  47. SM Moegenburg MJ Vanni (1991) ArticleTitleNutrient regeneration by zooplankton—effects on nutrient limitation of phytoplankton in a eutrophic lake. J Plankton Res 13 573–588

    Google Scholar 

  48. AE Murray CM Preston R Massana LT Taylor A Blakis K Wu EF DeLong (1998) ArticleTitleSeasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64 2585–2595 Occurrence Handle1:CAS:528:DyaK1cXkt1Ogsrw%3D Occurrence Handle9647834

    CAS  PubMed  Google Scholar 

  49. K Muylaert K Van der Gucht N Vloemans L De Meester 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 

  50. ML Pace JJ Cole (1996) ArticleTitleRegulation of bacteria by resources and predation tested in whole-lake experiments. Limnol Oceanogr 41 1448–1460

    Google Scholar 

  51. J Pinhassi A Hagstrom (2000) ArticleTitleSeasonal succession in marine bacterioplankton. Aquat Microb Ecol 21 245–256

    Google Scholar 

  52. K Porter Y Feig (1980) ArticleTitleThe use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25 943–948

    Google Scholar 

  53. T Posch K Simek J Vrba S Pernthaler J Nedoma B Sattler B Sonntag R Psenner (1999) ArticleTitlePredator-induced changes of bacterial size–structure and productivity studied on an experimental microbial community. Aquat Microb Ecol 18 235–246

    Google Scholar 

  54. L Riemann GF Steward F Azam (2000) ArticleTitleDynamics of bacterial community composition and activity during a mesocosm diatom bloom. AppI Environ Microbiol 66 578–587 Occurrence Handle10.1128/AEM.66.2.578-587.2000 Occurrence Handle1:CAS:528:DC%2BD3cXhtFeru7o%3D

    Article  CAS  Google Scholar 

  55. K Salonen P Kankaala T Tulonen T Hammar M James TR Metsala L Arvola (1992) ArticleTitlePlanktonic food-chains of a highly humic lake. 2. A mesocosm experiment in summer during dominance of heterotrophic processes. Hydrobiologia 229 143–157 Occurrence Handle1:CAS:528:DyaK38XkslGrtLc%3D

    CAS  Google Scholar 

  56. H Schafer 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

    Google Scholar 

  57. K Simek D Babenzien T Bittl R Koschel M Macek J Nedoma J Vrba (1998) ArticleTitleMicrobial food webs in an artificially divided acidic bog lake. Int Rev Hydrobiol 83 3–18 Occurrence Handle1:CAS:528:DyaK1cXhsVelsLs%3D

    CAS  Google Scholar 

  58. K Simek P Hartman J Nedoma J Pernthaler D Springmann J Vrba R Psenner (1997) ArticleTitleCommunity structure, picoplankton grazing and zooplankton control of heterotrophic nanoflagellates in a eutrophic reservoir during the summer phytoplankton maximum. Aquat Microb Ecol 12 49–63

    Google Scholar 

  59. K Simek K Hornak M Masin U Christaki J Nedoma MG Weinbauer JR Dolan (2003) ArticleTitleComparing the effects of resource enrichment and grazing on a bacterioplankton community of a meso-eutrophic reservoir. Aquat Microb Ecol 31 123–135

    Google Scholar 

  60. VH Smith (2002) ArticleTitleEffects of resource supplies on the structure and function of microbial communities. Ant Van Leeuwen 81 99–106 Occurrence Handle10.1023/A:1020533727307 Occurrence Handle1:CAS:528:DC%2BD38Xns1Sgs7Y%3D

    Article  CAS  Google Scholar 

  61. U Sommer (1989) Plankton Ecology: Succession in Plankton Communities Springer-Verlag New York

    Google Scholar 

  62. U Sommer ZM Gliwicz W Lampert A Duncan (1986) ArticleTitleThe PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol 106 433–471

    Google Scholar 

  63. Chemical Limnology of North Temperate Lakes Primary Study Lakes, North Temperate Lakes Long Term Ecological Research program, NSF (http://lter.limnology.wisc.edu), Stanley EH, Center for Limnology, University of Wisconsin–Madison

  64. DK Stoecker (1999) ArticleTitleMixotrophy among dinoflagellates. J Eukaryot Microbiol 46 397–401

    Google Scholar 

  65. L Stone RSJ Weisburd (1992) ArticleTitlePositive feedback in aquatic ecosystems. Trends Ecol Evol 7 263–267 Occurrence Handle10.1016/0169-5347(92)90172-8

    Article  Google Scholar 

  66. RD Tadonleke LB Jugnia T Sime-Ngando J Devaux JC Romagoux (2002) ArticleTitleFood web structure in the recently flooded Sep Reservoir as inferred from phytoplankton population dynamics and living microbial biomass. Microb Ecol 43 67–81 Occurrence Handle10.1007/s00248-001-1015-7 Occurrence Handle1:CAS:528:DC%2BD38XjslGhtrw%3D Occurrence Handle11984630

    Article  CAS  PubMed  Google Scholar 

  67. EJ van Hannen W Mooij MP van Agterveld 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

    Google Scholar 

  68. MG Weinbauer MG Hofle (1998) ArticleTitleDistribution and life strategies of two bacterial populations in a eutrophic lake. Appl Environ Microbiol 64 3776–3783 Occurrence Handle1:CAS:528:DyaK1cXms1ent7k%3D Occurrence Handle9758799

    CAS  PubMed  Google Scholar 

  69. M Weiss M Simon (1999) ArticleTitleConsumption of labile dissolved organic matter by limnetic bacterioplankton: the relative significance of amino acids and carbohydrates. Aquat Microbiol Ecol 17 1–12

    Google Scholar 

  70. AC Yannarell AD Kent GH Lauster TK Kratz EW Triplett (2003) ArticleTitleTemporal patterns in bacterial communities in three temperate lakes of different trophic status. Microb Ecol 46 391–405 Occurrence Handle10.1007/s00248-003-1008-9 Occurrence Handle1:STN:280:DC%2BD2c%2FitlKgsA%3D%3D Occurrence Handle12904915

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the NTL-LTER for logistical support and L. Graham and J. Rusak for helpful discussions during the preparation of this manuscript. This work was funded by NSF grants MCB-9977903, MCB-0401987, DEB-9632853, and DEB-0217533. This work was also supported by the Florida Agricultural Experiment Station, and approved as Journal Series No. R-10353.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E.W. Triplett.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kent, A., Jones, S., Yannarell, A. et al. Annual Patterns in Bacterioplankton Community Variability in a Humic Lake. Microb Ecol 48, 550–560 (2004). https://doi.org/10.1007/s00248-004-0244-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-004-0244-y

Keywords

Navigation