Microbial Ecology

, Volume 52, Issue 2, pp 358–364 | Cite as

Bacterioplankton Growth and Nutrient Use Efficiencies Under Variable Organic Carbon and Inorganic Phosphorus Ratios

  • Mats Jansson
  • Ann-Kristin Bergström
  • David Lymer
  • Katarina Vrede
  • Jan Karlsson
Article

Abstract

We carried out enclosure experiments in an unproductive lake in northern Sweden and studied the effects of enrichment with different dissolved organic carbon (glucose)/inorganic phosphorous (DOC/Pi) ratios on bacterioplankton production (BP), growth efficiency (BGE), nutrient use efficiency (BNUE), growth rate, and specific respiration. We found considerable variation in BP, BGE, and BNUE along the tested DOC/Pi gradient. BGE varied between 0.87 and 0.24, with the highest values at low DOC/Pi ratios. BNUE varied between 40 and 9 g C g P−1, with high values at high DOC/Pi ratios. More DOC was thus allocated to growth when bacteria tended to be C-limited, and to respiration when bacteria were P-limited. Specific respiration was positively correlated with bacterial growth rate throughout the gradient. It is therefore possible that respiration was used to support growth in P-limited bacteria. The results indicated that BP can be limited by Pi when BNUE is at its maximum, by organic C when BGE is at its maximum, and by dual organic C and Pi limitation when BNUE and BGE have suboptimal values.

References

  1. 1.
    Arvola, L, Tulonen, T (1998) Effects of allochthonous dissolved organic matter and inorganic nutrients on the growth of bacteria and algae from a highly humic lake. Environ Int 24: 509–520CrossRefGoogle Scholar
  2. 2.
    Bell, R, Ahlgren, GM, Ahlgren, I (1983) Estimating bacterioplankton production by measuring (H)-thymidine incorporation in a eutrophic lake. Microbiology 45: 1709–1721Google Scholar
  3. 3.
    Biddanda, BM, Ogdahl, M, Cotner, J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46: 730–739CrossRefGoogle Scholar
  4. 4.
    Chrzanowski, TH, Kyle, M (1995) Ratios of carbon, nitrogen and phosphorus in Pseudomonas fluorescence as a model for bacterial element ratios and nutrient regeneration. Aquat Microb Ecol 10: 115–122CrossRefGoogle Scholar
  5. 5.
    Currie, DJ, Kalff, J (1984) A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus. Limnol Oceanogr 29: 298–310CrossRefGoogle Scholar
  6. 6.
    del Giorgio, PA, Cole, JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29: 503–541CrossRefGoogle Scholar
  7. 7.
    Eiler, A, Langenheder, S, Bertilsson, S, Tranvik, LJ (2003) Heterotrophic bacterial growth efficiency and community structure at different natural organic carbon concentrations. Appl Environ Microbiol 69: 3701–3709PubMedCrossRefGoogle Scholar
  8. 8.
    Elser, JJ, Sterner, RW, Gorokhova, E (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3: 540–550CrossRefGoogle Scholar
  9. 9.
    Fagerbakke, KM, Heldal, M, Norland, S (1996) Content of carbon, nitrogen, oxygen, sulphur and phosphorus in native and cultured bacteria. Aquat Microb Ecol 10: 15–27CrossRefGoogle Scholar
  10. 10.
    Granéli, W, Bertilsson, S, Philibert, A (2004) Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquat Sci 66: 430–439CrossRefGoogle Scholar
  11. 11.
    Jansson, M (1993) Uptake, exchange and excretion of orthophosphate in phosphate-starved Scenedesmus quadricauda and Pseudomonas K7. Limnol Oceanogr 38: 1162–1178CrossRefGoogle Scholar
  12. 12.
    Jansson, M, Karlsson, J, Blomqvist, P (2003) Allochthonous organic carbon decreases pelagic energy mobilization in lakes. Limnol Oceanogr 48: 1711–1716CrossRefGoogle Scholar
  13. 13.
    Karlsson, J, Jansson, M, Jonsson, A (2002) Similar relationships between pelagic primary and bacterial production in clearwater and humic lakes. Ecology 83: 2902–2910Google Scholar
  14. 14.
    Khosmanesh, A, Hart, BT, Duncand, A, Becket, R (2002) Luxury uptake of phosphorus by sediment bacteria. Water Res 36: 774–778CrossRefGoogle Scholar
  15. 15.
    Lennon, JT, Pfaff, LE (2005) Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquat Microb Ecol 39: 107–119CrossRefGoogle Scholar
  16. 16.
    Makino, W, Cotner, JB (2004) Elemental stoichiometry of a heterotrophic bacterial community in a freshwater lake: implications for growth- and resource-dependant variations. Aquat Microbial Ecol 34: 33–41CrossRefGoogle Scholar
  17. 17.
    Neijssel, OM, Tempest, DW (1976) Bioenergetic aspects of aerobic growth of Klebsiells aerogenes NCTC in carbon-limited and carbon-sufficient culture. Arch Microbiol 107: 215–221PubMedCrossRefGoogle Scholar
  18. 18.
    Russel, JB, Cook, GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59: 48–62Google Scholar
  19. 19.
    Schindler, DW, Schmidt, RV, Reid, RA (1972) Acidification and548 bubbling as an alternative to filtration in determining phytoplankton production by the 14C method. J Fish Res Board Can 29: 1627–1631Google Scholar
  20. 20.
    Simon, M, Azam, F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201–213CrossRefGoogle Scholar
  21. 21.
    Smith, DC, Azam, F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6: 107–114Google Scholar
  22. 22.
    Smith, EM, Prairie, YT (2004) Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol Oceanogr 49: 137–147CrossRefGoogle Scholar
  23. 23.
    Sterner, RW, Elser, JJ, Fee, EJ, Guildford, SJ, Chrzanowski, TH (1997) The light:nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and process. Am Nat 150: 663–683CrossRefPubMedGoogle Scholar
  24. 24.
    Tempest, DW, Neijssel, OM (1978) Eco-physiological aspects of microbial growth in aerobic nutrient limited environments. Adv Microb Ecol 2: 105–153Google Scholar
  25. 25.
    Vadstein, O (2000) Heterotrophic, planktonic bacteria and cycling of phosphorus–phosphorus requirements, competitive ability, and food web interactions. In: Schink, B (Ed.) Advances in Microbial Ecology. Kluwer Academic Publishers/Plenum. New York, pp 115–167Google Scholar
  26. 26.
    Vitousek, P (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119: 553–572CrossRefGoogle Scholar
  27. 27.
    Wang, L, Miller, TD, Priscu, JC (1992) Bacterioplankton nutrient deficiency in a eutrophic lake. Arch Hydrobiol 125: 423–439Google Scholar
  28. 28.
    Vrede, K, Heldal, M, Norland, S, Bratbak, G (2002) Elemental composition (C, N, P) and cell volume of exponentially growing and nutrient-limited bacterioplankton. Appl Environ Microbiol 68: 2965–2971PubMedCrossRefGoogle Scholar
  29. 29.
    Vrede, K (1996) Regulation of bacterioplankton production and biomass in an oligotrophic clearwater lake—the importance of the phytoplankton community. J Plankton Res 18: 1009–1032CrossRefGoogle Scholar
  30. 30.
    Vrede, K (2005) Nutrient and temperature limitation of bacterioplankton growth in temperate lakes. Microb Ecol 49: 245–256PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Mats Jansson
    • 1
  • Ann-Kristin Bergström
    • 1
  • David Lymer
    • 2
  • Katarina Vrede
    • 2
  • Jan Karlsson
    • 3
  1. 1.Department of Ecology and Environmental ScienceUniversity of UmeåUmeåSweden
  2. 2.Limnology, Department of Ecology and Evolution, Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  3. 3.Climate Impacts Research Centre (CIRC), Department of Ecology and Environmental ScienceUmeå UniversityUmeåSweden

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