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Regulation of planktonic bacterial growth rates: The effects of temperature and resources

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Abstract

We examined the potential limitation of bacterial growth by temperature and nutrients in a eutrophic lake. Dilution cultures from winter and summer were incubated at both high (>20°C) and low (4°C) temperatures and enriched with various combinations of organic carbon (C), inorganic nitrogen (N), and inorganic phosphorus (P). Bacterial abundance, 3H-thymidine incorporation, and 3H-leucine incorporation were measured over the growth cycle. For both winter and summer assemblages, low temperature limited growth even when resources (C, N, and P) were added. When temperature was adequate, bacterial growth in dilution cultures was co-limited by C, N, and P Additions of either C, P, or N and P alone provide little or only modest stimulation of growth, suggesting that under in situ conditions both nutrients and organic carbon limit bacterial growth. Our results provide little evidence of seasonal adaptation to low temperatures for bacterial communities in temperate lakes. Instead, bacterial growth appears to be temperature limited during winter and resource limited during summer. We propose that, in general, bacterial growth rates are temperature dependent up to a threshold, but that the patterns of change across temperature gradients are resource dependent, such that temperature has little effect on growth in resource-rich environments but a strong effect in resource-poor environments.

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References

  1. Barillier A, Garnier J (1993) Influence of temperature and substrate concentration on bacterial growth yield in Seine River water batch cultures. Appl Environ Microbiol 59:1678–1682

    Google Scholar 

  2. Bell RT (1993) Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp 495–503

    Google Scholar 

  3. Bell RT, Vrede K, Setensdotter U, Blomqvist P (1993) Stimulation of the microbial food web in a oligotrophic, slightly acidified lake. Limnol Oceanogr 38:1532–1538

    Google Scholar 

  4. Bird DF, Karl DM (1989) Microbial incorporation of exogenous thymidine and glutamic acid in surface waters of the Bransfield Strait: a RACER analysis. Antarct J US 23:119–120

    Google Scholar 

  5. Bird DF, Karl DM (1991) Spatial patterns of glutamate and thymidine assimilation in Bransfield Strait, Antarctica during and following the austral spring bloom. Deep-Sea Res 38:1057–1075

    Google Scholar 

  6. Chin-Leo G, Kirchman DL (1988) Estimating bacterial production in marine waters from the simultaneous incorporation of thymidine and leucine. Appl Environ Microbiol 54:1934–1939

    Google Scholar 

  7. Cole JJ, Pace ML. Bacterial secondary production in oxic and anoxic fresh waters. Limnol Oceanogr in press.

  8. Cole JJ, Pace ML, Caraco NF, Steinhart GS (1993) Bacterial biomass and cell size distributions in lakes: more and larger cells in anoxic waters. Limnol Oceanogr 38:1627–1632

    Google Scholar 

  9. Coveney MF, Wetzel RG (1992) Effects of nutrients on specific growth rate of bacterioplankton in oligotrophic lake water cultures. Appl Environ Microbiol 58:150–156

    Google Scholar 

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

    Google Scholar 

  11. Ducklow HW Kirchman DL, Quinby HL (1992) Bacterioplankton cell growth and macromolecular synthesis in seawater cultures during the North Atlantic spring phytoplankton bloom, May, 1989. Microb Ecol 24:125–144

    Google Scholar 

  12. Ducklow HW Shiah FK (1993) Bacterial production in estuaries. In: Ford TE (ed) Aquatic microbiology: an ecological approach. Blackwell Scientific, Boston, pp 261–287

    Google Scholar 

  13. Elser JJ, Marzolf ER, Goldman CR (1990) Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. Can J Fish Aquat Sci 47:1468–1477

    Google Scholar 

  14. Ferguson RL, Buckley EN, Palumbo AV (1984) Response of marine bacterioplankton to differential filtration and confinement. Appl Environ Microbiol 47:49–55

    CAS  PubMed  Google Scholar 

  15. Fuhrman JA, Azam F (1980) Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl Environ Microbiol 39:1085–1095

    Google Scholar 

  16. Glibert PM, Miller CA, Garside C, Roman MR, McManus GB (1992) NH4 + regeneration and grazing: interdependent processes in size-fractionated 15NH4 + experiments. Mar Ecol Prog Ser 82:65–74

    Google Scholar 

  17. Goldman JC, Caron DA, Dennett MR (1987) Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C:N ratio. Limnol Oceanogr 32:1239–1252

    Google Scholar 

  18. Hanson RB, Shafer D, Ryan T, Pope DH, Lowery HK (1983) Bacterioplankton in Antarctic ocean waters during late austral winter: abundance, frequency of dividing cells and estimates of production. Appl Environ Microbiol 45:1622–1632

    Google Scholar 

  19. Hoch MP, Kirchman DL (1993) Seasonal and inter-annual variability in bacterial production and biomass in a temperate estuary. Mar Ecol Prog Ser 98:283–295

    Google Scholar 

  20. Hopkinson CS, Jr, Sherr B, Wiebe WJ (1989) Size fractionated metabolism of coastal microbial plankton. Mar Ecol Prog Ser 51:155–166

    Google Scholar 

  21. Kamphake LJ, Hannah SA, Cohen JM (1967) Automated analyses for nitrate by hydrazine reduction. Water Res 1:206–209

    Google Scholar 

  22. Kirchman DL (1990) Limitation of bacterial growth by dissolved organic matter in the subarctic Pacific. Mar Ecol Prog Ser 62:47–54

    Google Scholar 

  23. Kirchman DL (1993) Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in Aquatic Microbial Ecology, Lewis Publishers, Boca Raton, pp 509–512

    Google Scholar 

  24. Kirchman DL, Hoch MP (1988) Bacterial production in the Delaware Bay estuary estimated from thymidine and leucine incorporation rates. Mar Ecol Prog Ser 45:169–178

    Google Scholar 

  25. Kramer H, Moed JR, De Haan H (1990) Nitrogen analyses in eutrophic, alkaline, peaty waters: a comparison of different method to analyze ammonia nitrogen. Water Res 24:221–224

    Google Scholar 

  26. Li WKW Dickie PM (1987) Temperature characteristics of photosynthetic and heterotrophic activities: seasonal variations in temperate microbial plankton. Appl Environ Microbiol 53:2282–2295

    Google Scholar 

  27. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  28. Morris DP, Lewis WM (1992) Nutrient limitation of bacterioplankton growth in Lake Dillon, Colorado. Limnol Oceanogr 37:1179–1192

    Google Scholar 

  29. Pace ML (1993) Heterotrophic microbial processes. In: Carpenter SR, Kitchell JF (eds) The trophic cascade in lakes. Cambridge University Press, New York, pp 252–277

    Google Scholar 

  30. Pace ML, Cole JJ (1993) Primary and bacterial production in lakes: are they coupled over depth? J Plank Res 16:661–672

    Google Scholar 

  31. Pace ML, Cole JJ (1994) Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb Ecol 28:181–193

    Google Scholar 

  32. Pace ML, McManus GB, Findlay SEG (1990) Planktonic community structure determines the fate of bacterial production in a temperate lake. Limnol Oceanogr 35:795–808

    Google Scholar 

  33. Pomeroy LR, Deibel D (1986) Temperature regulation of bacterial activity during the spring bloom in Newfoundland coastal waters. Science 233:359–361

    Google Scholar 

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

    Google Scholar 

  35. Scavia DL, Laird GA (1987) Bacterioplankton in Lake Michigan: dynamics, controls, and significance to carbon flux. Limnol Oceanogr 32:1017–1033

    Google Scholar 

  36. Servais P, Gamier J (1993) Contribution of heterotrophic bacteria to the carbon budget of the River Seine (France). Microb Ecol 25:19–33

    Google Scholar 

  37. Sherr B, Sherr EB, Hopkinson CS (1988) Trophic interactions within pelagic microbial communities: indicators of feedback regulation of carbon flow. Hydrobiologia 159:19–26

    Google Scholar 

  38. Solorzano L (1969) Determination of ammonia in natural waters by the phenol (+) hypochlorite method. Limnol Oceanogr 14:799–801

    Google Scholar 

  39. Steel RGD, Torrie JH (1980) Principles and procedures of statistics. 2nd ed. McGraw-Hill, New York

    Google Scholar 

  40. Toolan T, Wehr JD, Findlay S (1991) Inorganic phosphorus stimulation of bacterioplankton production in a meso-eutrophic lake. Appl Environ Microbiol 57:2074–2078

    Google Scholar 

  41. Tulonen T (1993) Bacterial production in a mesohumic lake estimated from [14C]leucine incorporation rate. Microb Ecol 26:201–217

    Google Scholar 

  42. Turley C (1993) Direct estimates of bacterial numbers in seawater samples without incurring cell loss dues to sample storage. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology, Lewis Publishers, Boca Raton, pp 143–147

    Google Scholar 

  43. Watanabe Y, Goldman CR (1984) Heterotrophic bacterial community in oligotrophic Lake Tahoe. Int Ver Theor Angew Limnol Verb 22:584–590

    Google Scholar 

  44. White PA, Kalff J, Rasmussen JB, Gasol JM (1991) The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microb Ecol 21:99–118

    Google Scholar 

  45. Wiebe WJ, Sheldon WM, Jr, Pomeroy LIZ (1992) Bacterial growth in the cold: evidence for an enhanced substrate requirement. Appl Environ Microbiol 58:359–364

    Google Scholar 

  46. Wiebe WJ, Sheldon WM, Jr, Pomeroy LR (1993) Evidence for an enhanced substrate requirement by marine mesophilic bacterial isolates at minimal growth temperatures. Microb Ecol 25:151–159

    Google Scholar 

  47. Wikner J, Hagström A (1991) Annual study of bacterioplankton community dynamics. Limnol Oceanogr 36:1313–1324

    Google Scholar 

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Authors and Affiliations

  1. Departament d'Ecologia and Centre de Recerca d'Alta Muntanya, Universitat de Barcelona, Avgda. Diagonal 645, 08028, Barcelona, Spain

    M. Felip

  2. Institute of Ecosystem Studies, Box AB, 12545, Millbrook, New York, USA

    M. L. Pace & J. J. Cole

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  1. M. Felip
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  2. M. L. Pace
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  3. J. J. Cole
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Correspondence to: Marisol Felip

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Felip, M., Pace, M.L. & Cole, J.J. Regulation of planktonic bacterial growth rates: The effects of temperature and resources. Microb Ecol 31, 15–28 (1996). https://doi.org/10.1007/BF00175072

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  • DOI: https://doi.org/10.1007/BF00175072

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