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Temporal Patterns in Bacterial Communities in Three Temperate Lakes of Different Trophic Status

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Abstract

Despite considerable attention in recent years, the composition and dynamics of lake bacterial communities over annual time scales are poorly understood. This study used automated ribosomal intergenic spacer analysis (ARISA) to explore the patterns of change in lake bacterial communities in three temperate lakes over 2 consecutive years. The study lakes included a humic lake, an oligotrophic lake, and a eutrophic lake, and the epilimnetic bacterial communities were sampled every 2 weeks. The patterns of change in bacterial communities indicated that seasonal forces were important in structuring the behavior of the bacterial communities in each lake. All three lakes had relatively stable community composition in spring and fall, but summer changes were dramatic. Summertime variability was often characterized by recurrent drops in bacterial diversity. Specific ARISA fragments derived from these lakes were not constant among lakes or from year to year, and those fragments that did recur in lakes in different years did not exhibit the same seasonal pattern of recurrence. Nonetheless, seasonal patterns observed in 2000 were fairly successful predictors of the rate of change in bacterial communities and in the degree of autocorrelation of bacterial communities in 2001. Thus, seasonal forces may be important structuring elements of these systems as a whole even if they are uncoupled from the dynamics of the individual system components.

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References

  1. PE Applied Biosystems (1996) ABI Prism Genotyper

  2. PE Applied Biosystems (2000) ABI Prism GeneScan Analysis

  3. TFH Allen SM Bartell JF Koonce (1977) ArticleTitleMultiple stable configurations in ordination of phytoplankton community change rates. Ecology 58 1076–1084

    Google Scholar 

  4. R Amann BM Fuchs S Behrens (2001) ArticleTitleThe identification of microorganisms by fluorescence in situ hybridisation. Curr Opin Biotechnol 12 231–236 Occurrence Handle1:CAS:528:DC%2BD3MXkt12lu74%3D Occurrence Handle11404099

    CAS  PubMed  Google Scholar 

  5. 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 

  6. B Biddanda M Ogdahl J Cotner (2001) ArticleTitleDominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46 730–739

    Google Scholar 

  7. J Borneman EW Triplett (1997) ArticleTitleMolecular microbial diversity in soils from Eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63 2647–2653 Occurrence Handle1:CAS:528:DyaK2sXktlektLg%3D Occurrence Handle9212415

    CAS  PubMed  Google Scholar 

  8. DA Caron (1994) ArticleTitleInorganic nutrients, bacteria, and the microbial loop. Microb Ecol 28 295–298

    Google Scholar 

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

    Google Scholar 

  10. KR Clarke RN Gorley (2001) PRIMER 5 for Windows PRIMER-E Ltd. Plymouth, UK

    Google Scholar 

  11. KR Clarke RH Green (1988) ArticleTitleStatistical design and analysis for a “biological effects” study. Mar Ecol Prog Ser 46 213–226 Occurrence Handle1:CAS:528:DC%2BD3MXjsl2iurw%3D Occurrence Handle11285313

    CAS  PubMed  Google Scholar 

  12. KR Clarke RM Warwick (1998) ArticleTitleQuantifying structural redundancy in ecological communities. Oecologia 113 278–289 Occurrence Handle10.1007/s004420050379

    Article  Google Scholar 

  13. JJ Cole S Findlay ML Pace (1988) ArticleTitleBacterial production in fresh and saltwater: a cross-system overview. Mar Ecol Prog Ser 43 1–10

    Google Scholar 

  14. JJ Cole GL Likens EE Gene JE Hobbie (1984) ArticleTitleDecomposition of planktonic algae in an oligotrophic lake. Oikos 42 257–266 Occurrence Handle1:CAS:528:DyaL2cXksF2ktL8%3D

    CAS  Google Scholar 

  15. R Danovaro D Marrale N Della Croce A Dell’Anno M Fabiano (1998) ArticleTitleHeterotrophic nanoflagellates, bacteria, and labile organic compounds in continental shelf and deep-sea sediments of the Eastern Mediterranean. Microb Ecol 35 244–255

    Google Scholar 

  16. HW Ducklow CA Carlson (1992) Oceanic bacterial production. KC Marshall (Eds) Advances in Microbial Ecology Plenum Press New York 113–181

    Google Scholar 

  17. M Felip ML Pace JJ Cole (1996) ArticleTitleRegulation of planktonic bacterial growth rates: the effects of temperature and resources. Microb Ecol 31 15–28

    Google Scholar 

  18. JG Field KR Clarke RM Warwick (1982) ArticleTitleA practical strategy for analysing multispecies distribution patterns. Mar Ecol Prog Ser 8 37–52

    Google Scholar 

  19. 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

    Google Scholar 

  20. MM Fisher JL Klug G Lauster M Newton EW Triplett (2001) ArticleTitleEffects of resources and trophic interactions on freshwater bacterioplankton. Microb Ecol 41 82–82

    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. FO Glöckner BM Fuchs R Amann (1999) ArticleTitleBacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65 3721–3726

    Google Scholar 

  23. 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–+

    Google Scholar 

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

    Google Scholar 

  25. LA Hansson LG Rudstam TB Johnson P Soranno Y Allen (1994) ArticleTitlePatterns in algal recruitment from sediment to water in a dimictic, eutrophic lake. Can J Fish Aqua Sci 51 2825–2833

    Google Scholar 

  26. 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 

  27. SH Hurlbert (1984) ArticleTitlePseudoreplication and the design of ecological field experiments. Ecol Monogr 54 187–211

    Google Scholar 

  28. K Šimek P Kojecká J Nedoma P Hartman J Vrba JR Dolan (1999) ArticleTitleShifts in bacterial community composition associated with different microzooplankton size fractions in a eutrophic reservoir. Limnol Oceanogr 44 1634–1644

    Google Scholar 

  29. E Jaspers K Nauhaus H Cypionka J Overmann (2001) ArticleTitleMultitude and temporal variability of ecological niches as indicated by the diversity of cultivated bacterioplankton. FEMS Microbiol Ecol 36 153–164

    Google Scholar 

  30. 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

    Google Scholar 

  31. 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

    Google Scholar 

  32. DL Kirchman (1994) ArticleTitleThe uptake of inorganic nutrients by heterotrophic bacteria. Microb Ecol 28 255–271 Occurrence Handle1:CAS:528:DyaK2MXit1Wktbo%3D

    CAS  Google Scholar 

  33. CL Kitts (2001) ArticleTitleTerminal restriction fragment patterns: a tool for comparing microbial communities and assessing community dynamics. Curr Issues Intest Microbiol 2 17–25 Occurrence Handle1:CAS:528:DC%2BD3MXjvVyiu7o%3D Occurrence Handle11709853

    CAS  PubMed  Google Scholar 

  34. A Konopka T Bercot C Nakatsu (1999) ArticleTitleBacterioplankton community diversity in a series of thermally stratified lakes. Microb Ecol 38 126–135

    Google Scholar 

  35. Physical limnology of the North Temperate Lakes Primary Study lakes, North Temperate Lakes Long Term Ecological Research Program, NSF (http://www.limnology.wisc.edu ), Kratz TK, Center for Limnology, University of Wisconsin–Madison

  36. C Kruk N Mazzeo G Lacerot CS Reynolds (2002) ArticleTitleClassification schemes for phytoplankton: a local validation of a functional approach to the analysis of species temporal replacement. J Plankton Res 24 901–912 Occurrence Handle10.1093/plankt/24.9.901

    Article  Google Scholar 

  37. JB Kruskal (1964) ArticleTitleMultidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29 1–27

    Google Scholar 

  38. JB Kruskal M Wish (1978) Multidimensional Scaling Sage Publications Beverly Hills, CA

    Google Scholar 

  39. DJ Lane (1991) 16S/23S rRNA sequencing. E Stackebrandt M Goodfellow (Eds) Nucleic Acid Techniques in Bacterial Systematics Wiley & Sons Chichester, UK

    Google Scholar 

  40. S Langenheder K Jürgens (2001) ArticleTitleRegulation of bacterial biomass and community structure by metazoan and protozoan predation. Limnol Oceanogr 46 121–134 Occurrence Handle1:STN:280:By6C2svkvFw%3D Occurrence Handle2006870

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  42. ES Lindström E Leskinen (2002) ArticleTitleDo neighboring lakes share common taxa of bacterioplankton? Comparison of the 16S rDNA fingerprints and sequences from three geographic regions. Microb Ecol 44 1–9

    Google Scholar 

  43. WT Liu TL Marsh H Cheng LJ Forney (1997) ArticleTitleCharacterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63 4516–4522 Occurrence Handle1:CAS:528:DyaK2sXnt12ntbs%3D Occurrence Handle9361437

    CAS  PubMed  Google Scholar 

  44. 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 

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

    Google Scholar 

  46. KV Mardia JT Kent JM Biddy (1979) Multivariate Analysis Academic Press London

    Google Scholar 

  47. McCune B, Grace JB (2002) Analysis of Ecological Communities. MjM Software Design, Gleneden Beach, Oregon

  48. BA Methé WD Hiorns JP Zehr (1998) ArticleTitleContrasts between marine and freshwater bacterial community composition: Analyses of communities in Lake George and six other Adirondack lakes. Limnol Oceanogr 43 368–374 Occurrence Handle1:CAS:528:DyaK1cXjvFWisro%3D

    CAS  Google Scholar 

  49. BA Methé JP Zehr (1999) ArticleTitleDiversity of bacterial communities in Adirondack lakes: do species assemblages reflect lake water chemistry? Hydrobiologia 401 77–96 Occurrence Handle10.1023/A:1003782209607

    Article  Google Scholar 

  50. AM Osborn ERB Moore KN Timmis (2000) ArticleTitleAn evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2 39–50 Occurrence Handle10.1046/j.1462-2920.2000.00081.x Occurrence Handle1:CAS:528:DC%2BD3cXhs12ht7k%3D Occurrence Handle11243261

    Article  CAS  PubMed  Google Scholar 

  51. MF Polz CM Cavanaugh (1998) ArticleTitleBias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64 3724–3730 Occurrence Handle1:CAS:528:DyaK1cXms1entrc%3D Occurrence Handle9758791

    CAS  PubMed  Google Scholar 

  52. CS Reynolds (2000) ArticleTitlePhytoplankton designer—or how to predict compositional responses to trophic-state change. Hydrobiologia 424 123–132 Occurrence Handle10.1023/A:1003913330889

    Article  Google Scholar 

  53. CS Reynolds V Huszar C Kruk L Naselli-Flores S Melo (2002) ArticleTitleTowards a functional classification of the freshwater phytoplankton. J Plankton Res 24 417–428 Occurrence Handle10.1093/plankt/24.5.417

    Article  Google Scholar 

  54. T SimeNgando (1997) ArticleTitleViruses in aquatic ecosystems. A review. Anee Biol 36 181–210

    Google Scholar 

  55. M Simon C Byong F Azam (1992) ArticleTitleSignificance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications. Mar Ecol Prog Ser 86 103–110

    Google Scholar 

  56. U Sommer (1993) ArticleTitlePhytoplankton competition in Plußsee: a field test of the resource-ratio hypothesis. Limnol Oceanogr 38 838–845 Occurrence Handle1:CAS:528:DyaK2cXit1GqtLY%3D

    CAS  Google Scholar 

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

  58. R Stepanauskas H Edling LJ Tranvik (1999) ArticleTitleDifferential dissolved organic nitrogen availability and bacterial aminopeptidase activity in limnic and marine waters. Microb Ecol 38 264–272

    Google Scholar 

  59. M Suzuki MS Rappe SJ Giovannoni (1998) ArticleTitleKinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity. Appl Environ Microbiol 64 4522–4529

    Google Scholar 

  60. MT Suzuki SJ Giovannoni (1996) ArticleTitleBias caused by template annealing in the amplification of mixtures 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 

  61. P Tuomi T Torsvik M Heldal G Bratbak (1997) ArticleTitleBacterial population dynamics in a meromictic lake. Appl Environ Microbiol 63 2181–2188

    Google Scholar 

  62. X Vila CA Abella JB Figueras JP Hurley (1998) ArticleTitleVertical models of phototrophic bacterial distribution in the metalimnetic microbial communities of several freshwater North-American kettle lakes. FEMS Microbiol Ecol 25 287–299

    Google Scholar 

  63. X Vila XP Cristina CA Abella JP Hurley (1999) ArticleTitleEffects of gilvin on the composition and dynamics of metalimnetic communities of phototrophic bacteria in freshwater North-American lakes. J Appl Microbiol 85 138S–150S

    Google Scholar 

  64. P Weiss B Schweitzer R Amann M Simon (1996) ArticleTitleIdentification in situ and dynamics of bacteria on limnetic organic aggregates (lake snow). Appl Environ Microbiol 62 1998–2005

    Google Scholar 

  65. PA White J Kalff JB Rasmussen JM Gasol (1991) ArticleTitleThe effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microb Ecol 21 99–115

    Google Scholar 

  66. G Zwart WD Hiorns BA Methé MP Van Agterveld R Huismans SC Nold JP Zehr HJ Laanbroek (1998) ArticleTitleNearly identical 16S rRNA sequences recovered from lakes in North America and Europe indicate the existence of clades of globally distributed freshwater bacteria. Syst Appl Microbiol 21 546–556 Occurrence Handle1:STN:280:DyaK1M7itlyqug%3D%3D Occurrence Handle9924823

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank B. Benson, S. Lake, J. and L. Graham, S. Carpenter, D. Armstrong, and the NTL-LTER technicians for their valuable assistance with this manuscript. This work was funded by NSF grant DEB 9977903, awarded to the Center for Limnology at University of Wisconsin–Madison.

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Authors and Affiliations

  1. Center for Limnology, University of Wisconsin–Madison, Madison, WI 53706, USA

    A. C. Yannarell, A. D. Kent & G. H. Lauster

  2. Trout Lake Station, Center for Limnology, University of Wisconsin, 10810 County Highway N, Boulder Junction, WI 54512, USA

    T. K. Kratz

  3. Department of Agronomy, University of Wisconsin–Madison, Madison, WI 53706, USA

    E. W. Triplett

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  1. A. C. Yannarell
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  2. A. D. Kent
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  3. G. H. Lauster
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Correspondence to E. W. Triplett.

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Yannarell, A., Kent, A., Lauster, G. et al. Temporal Patterns in Bacterial Communities in Three Temperate Lakes of Different Trophic Status . Microb Ecol 46, 391–405 (2003). https://doi.org/10.1007/s00248-003-1008-9

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