Skip to main content
SpringerLink
Log in

Nutrient and Temperature Limitation of Bacterioplankton Growth in Temperate Lakes

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Limitation of bacterioplankton production by nutrients and temperature was investigated in eight temperate lakes in summer. Six of the lakes were resampled in autumn. The lakes differ in nutrient content, water color, and concentration of dissolved organic carbon. Nutrients (phosphorus, nitrogen, and organic carbon) were added alone and in all possible combinations to filtered lake water inoculated with bacteria from the lake. After incubation for 36–40 h at in situ temperatures (ranging from 7 to 20°C), the response in bacterioplankton production was determined. The effect of increased temperature on bacterioplankton growth was also tested. Bacterioplankton production was often limited by phosphorus alone, organic carbon alone, or the two in combination. Phosphorus limitation of bacterioplankton production was more common in the summer, whereas limitation by organic carbon was more frequently observed in the autumn. There was a close balance between limitation by phosphorus and organic carbon in the epilimnion in the summer. In the hypolimnion in the summer, bacterioplankton growth was primarily phosphorus-limited. The effect of phosphorus additions decreased with increasing phosphorus concentrations in the lakes. However, there were no correlations between the effect of added organic carbon and water color, dissolved organic carbon concentration, or phosphorus concentration. When temperature was low (in the hypolimnion in the summer, and throughout the water column in the autumn) temperature also limited bacterioplankton production. Thus, temperature and inorganic nutrients or organic compounds can limit bacterioplankton growth both alone and simultaneously. However, at low temperatures, temperature is the most important factor influencing bacterioplankton growth.

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

Similar content being viewed by others

References

  1. RT Bell (1993) Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine PF Kemp BF Sherry JJ Cole (Eds) Handbook of Methods in Aquatic Microbial Ecology Lewis Boca Raton, FL 495–503

    Google Scholar 

  2. RT Bell (1990) ArticleTitleAn explanation for the variability in the conversion factor deriving bacterial cell production from incorporation of [3H] thymidine Limnol Oceanogr 35 910–915

    Google Scholar 

  3. K Bendschneider RJ Robinson (1952) ArticleTitleA new spectrophotometric determination of nitrite in sea water J Mar Res 11 87–96

    Google Scholar 

  4. P Blomqvist RT Bell H Olofssor U Stensdotter K Vrede (1995) ArticleTitlePlankton and water chemistry in Lake Njupfatet before and after liming Can J Fish Aquat Sci 52 551–565

    Google Scholar 

  5. H Box WG Hunter JS Hunter (1978) Statistics for Experimenters John Wiley & Sons New York

    Google Scholar 

  6. G Bratbak TF Thingstad (1985) ArticleTitlePhytoplankton–bacteria interactions: an apparent paradox? Analysis of a model system with both competition and commensalism Mar Ecol Prog Ser 25 23–30

    Google Scholar 

  7. DA Caron E Lin Lim RW Sanders MR Dennet U-G Berninger (2000) ArticleTitleResponses of bacterioplankton and phytoplankton to organic carbon and inorganic nutrient additions in contrasting oceanic ecosystems Aquat Microb Ecol 22 175–184

    Google Scholar 

  8. TH Chrzanowski RW Sterner JJ Elser (1995) ArticleTitleNutrient enrichment and nutrient regeneration stimulate bacterioplankton growth Microb Ecol 29 221–230 Occurrence Handle10.1007/BF00164886

    Article  Google Scholar 

  9. WJ Conover (1980) Practical Nonparametric Statistics EditionNumber2 John Wiley & Sons New York

    Google Scholar 

  10. JB Cotner JW Ammerman ER Peele E Bentzer (1997) ArticleTitlePhosphorus-limited bacterioplankton growth in the Sargasso Sea Aquat Microb Ecol 13 141–149

    Google Scholar 

  11. MT Cottrell DL Kirchman (2000) ArticleTitleNatural assemblages of marine proteobacteria and members of the Cytophaga–Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter Appl Environ Microbiol 66 1692–1697 Occurrence Handle10.1128/AEM.66.4.1692-1697.2000 Occurrence Handle10742262

    Article  PubMed  Google Scholar 

  12. MF Coveney RG Wetzel (1995) ArticleTitleBiomass, production, and specific growth rate of bacterioplankton and coupling to phytoplankton in an oligotrophic lake Limnol Oceanogr 40 1187–1200

    Google Scholar 

  13. DJ Currie (1990) ArticleTitleLarge-scale variability and interactions among phytoplankton, bacterioplankton, and phosphorus Limnol Oceanogr 35 1437–1455

    Google Scholar 

  14. PA Giorgio Particledel G Scarborough (1995) ArticleTitleIncrease of the proportion of metabolically active bacteria along gradients of enrichment in freshwater and marine plankton: implications for estimates of bacterial growth and production J Plankton Res 17 1905–1924

    Google Scholar 

  15. JJ Elser BL Stable PR Hassett (1995) ArticleTitleNutrient limitation of bacterial growth and rates of bacterivory in lakes and oceans: a comparative study Aquat Microb Ecol 9 105–110

    Google Scholar 

  16. KM Fagerbakke M Heldal S Norland (1996) ArticleTitleContent of carbon, nitrogen, oxygen, sulphur and phosphorus in native aquatic and cultured bacteria Aquat Microb Ecol 10 15–27

    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 Occurrence Handle10.1007/BF00175072

    Article  Google Scholar 

  18. BM Fuchs MV Zubkoy K Saham PH Burkill R Amann (2000) ArticleTitleChanges in community composition during dilution cultures of maine bacterioplankton as assessed by flow cytometric and molecular biological techniques Environ Microbiol 2 191–201 Occurrence Handle10.1046/j.1462-2920.2000.00092.x Occurrence Handle11220305

    Article  PubMed  Google Scholar 

  19. W Goedkoop L Sonesten (1995) ArticleTitleLaborationsmanual för kemiska analyser av inlandsvatten och sediment [in Swedish] Scripta Limnologica Upsaliensia 1995 B 12

    Google Scholar 

  20. JP Grover TH Chrzanowski (2000) ArticleTitleSeasonal patterns of substrate utilization by bacterioplankton: case studies in four temperate lakes of different latitudes Aquat Microb Ecol 23 41–54

    Google Scholar 

  21. TB Gurung J Urabe (1999) ArticleTitleTemporal and vertical differences in factors limiting growth rate of heterotrophic bacterial in Lake Biwa Microb Ecol 38 IssueID2 136–145 Occurrence Handle10.1007/s002489900167 Occurrence Handle10441706

    Article  PubMed  Google Scholar 

  22. A-L Haglund E Törnblom B Boström L Tranvik (2002) ArticleTitleLarge differences in the fraction of active bacteria in plankton, sediments, and biofilms Microb Ecol 43 232–241 Occurrence Handle10.1007/s00248-002-2005-0 Occurrence Handle12023730

    Article  PubMed  Google Scholar 

  23. DO Hessen T Andersen A Lyche (1990) ArticleTitleCarbon metabolism in a humic lake: pool sizes and cycling through zooplankton Limnol Oceanogr 35 84–99

    Google Scholar 

  24. DO Hessen K Nygaard K Saloner A Vähätalo (1994) ArticleTitleThe effect of substrate stoichiometry on microbial activity and carbon degradation in humic lakes Environ Int 20 67–76 Occurrence Handle10.1016/0160-4120(94)90068-X

    Article  Google Scholar 

  25. M Jansson P Blomqvist A Jonsson A-K Bergström (1996) ArticleTitleNutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsk Limnol Oceanogr 41 1552–1559

    Google Scholar 

  26. 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 IssueID2 241–246 Occurrence Handle10.1093/plankt/fbh010

    Article  Google Scholar 

  27. R Massana P-A Carlos EO Casamayor JM Gasol (2001) ArticleTitleChanges in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters Limnol Oceanogr 46 1181–1188

    Google Scholar 

  28. C Matz K Jürgens (2003) ArticleTitleInteraction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community Microb Ecol 45 384–398 Occurrence Handle10.1007/s00248-003-2000-0 Occurrence Handle12704556

    Article  PubMed  Google Scholar 

  29. DP Morris WM Lewis SuffixJr (1992) ArticleTitleNutrient limitation of bacterioplankton growth in Lake Dillon, Colorado Limnol Oceanogr 37 1179–1192

    Google Scholar 

  30. DB Nedwell (1999) ArticleTitleEffect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature FEMS Microb Ecol 30 101–111 Occurrence Handle10.1016/S0168-6496(99)00030-6

    Article  Google Scholar 

  31. CA Ochs JJ Cole GE Likens (1995) ArticleTitlePopulation dynamics of bacterioplankton in an oligotrophic lake J Plankton Res 17 365–391

    Google Scholar 

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

    Google Scholar 

  33. LR Pomeroy WJ Wiebe (2001) ArticleTitleTemperature and substrates as interactive limiting factors for marine heterotrophic bacteria Aquat Microb Ecol 23 187–204

    Google Scholar 

  34. LR Pomeroy WJ Wiebe D Deibel JT Thompson GT Rowe JD Pakulaski (1991) ArticleTitleBacterial responses to temperature and substrate concentration during the Newfoundland spring bloom Mar Ecol Prog Ser 75 143–159

    Google Scholar 

  35. T Posch M Loferer-Krößbacher G Gad A Alfreider J Pernthaler R Psenner (2001) ArticleTitlePrecision of bacterioplankton biomass determination: a comparison of two fluorescent dyes, and of allomteric and linear volume-to-carbon conversion factors Aquat Microb Ecol 25 55–63

    Google Scholar 

  36. RW Sanders KG Porter SJ Bennett AE DeBiase (1989) ArticleTitleSeasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community Limnol Oceanogr 34 673–687

    Google Scholar 

  37. B Schweitzer M Simon (1995) ArticleTitleGrowth limitation of planktonic bacteria in a large mesotrophic lake Microb Ecol 30 89–104 Occurrence Handle10.1007/BF00184516

    Article  Google Scholar 

  38. M Simon 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 

  39. M Simon C Wünsch (1998) ArticleTitleTemperature control of bacterioplankton growth in a temperate large lake Aquat Microb Ecol 16 119–130

    Google Scholar 

  40. EM Smith YT Prairie (2004) ArticleTitleBacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability Limnol Oceanogr 49 137–147

    Google Scholar 

  41. M Søndergaard M Middelboe (1995) ArticleTitleA cross-system analysis of labile dissolved organic carbon Mar Ecol Prog Ser 118 283–294

    Google Scholar 

  42. TF Thingstad UL Zweife F Rassoulzadegan (1998) ArticleTitleP limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean Limnol Oceanogr 43 88–94

    Google Scholar 

  43. T Toolan JD Weh S Findlay (1991) ArticleTitleInorganic phosphorus stimulation of bacterioplankton production in a meso-eutrophic lake Appl Environ Microbiol 57 2074–2078

    Google Scholar 

  44. T Tulonen P Kankaala L Arvola A Ojala (2000) ArticleTitleGrowth and production of bacterioplankton in a deep mesotrophic boreal lake Arch Hydrobiol 147 311–325

    Google Scholar 

  45. O Vadstein (2000) ArticleTitleHeterotrophic, planktonic bacteria and cycling of phosphorus Phosphorus requirements, competitive ability, and food web interactions. Adv Microb Ecol 16 115–167

    Google Scholar 

  46. O Vadstein LM Olsen A Busch T Andersen HR Reinertsen (2003) ArticleTitleIs phosphorus limitation of planktonic heterotrophic bacteria and accumulation of degradable DOC a normal phenomenon in phosphorus-limited systems? A microcosm study FEMS Microb Ecol 1556 1–10

    Google Scholar 

  47. K Vrede (1999) ArticleTitleEffects of inorganic nutrients and zooplankton on the growth of heterotrophic bacterioplankton—enclosure experiments in an oligotrophic clearwater lake Aquat Microb Ecol 18 133–144

    Google Scholar 

  48. K Vrede (1996) ArticleTitleRegulation of bacterioplankton production and biomass in an oligotrophic clearwater lake—the importance of the phytoplankton community J Plankton Res 18 1009–1032

    Google Scholar 

  49. K Vrede M Heldal S Norland G Bratbak (2002) ArticleTitleThe elemental composition (C, N, P) and cell volume of exponentially growing and nutrient limited bacterioplankton Appl Environ Microbiol 68 2965–2971 Occurrence Handle10.1128/AEM.68.6.2965-2971.2002 Occurrence Handle12039756

    Article  PubMed  Google Scholar 

  50. K Vrede T Vrede A Isaksson A Karlsson (1999) ArticleTitleEffects of nutrients (P, N, C) and zooplankton on bacterioplankton and phytoplankton—a seasonal study Limnol Oceanogr 44 1616–1624

    Google Scholar 

  51. L Wang TD Miller JC Priscu (1992) ArticleTitleBacterioplankton nutrient deficiency in a eutrophic lake Arch Hydrobiol 125 423–439

    Google Scholar 

  52. JH Zar (1984) Biostatistical Analysis EditionNumber2 Prentice Hall Upper Saddle River, NJ

    Google Scholar 

  53. T Östling L Holqvist K Flärdh B Svenblad Å Jouper-Jaan S Kjelleberg (1993) Starvation and recovery of Vibrio. S Kjelleberg (Eds) Starvation in Bacteria Plenum Press New York 103–127

    Google Scholar 

Download references

Acknowledgments

Ulrika Stensdotter-Blomberg, Jan Johansson, Sandra Lindahl, Isabell Olevall, and Björn Vrede are acknowledged for help with fieldwork and/or analyses in the laboratory. Eva Lindström and Tobias Vrede and two anonymous reviewers are acknowledged for constructive comments on the manuscript. This study was financed by the Knut and Alice Wallenbergs Foundation, the Helge Ax:son Johnssons Foundation, the Foundation of Oscar and Lili Lamms Minne, and the Royal Swedish Academy of Science.

Author information

Authors and Affiliations

  1. Limnology/Department of Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 20, Uppsala, SE-752 36 , Sweden

    K. Vrede

Authors
  1. K. Vrede
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Vrede.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vrede, K. Nutrient and Temperature Limitation of Bacterioplankton Growth in Temperate Lakes. Microb Ecol 49, 245–256 (2005). https://doi.org/10.1007/s00248-004-0259-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-004-0259-4

Keywords

Search

Navigation