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.
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References
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: 509–520
Bell, R, Ahlgren, GM, Ahlgren, I (1983) Estimating bacterioplankton production by measuring (H)-thymidine incorporation in a eutrophic lake. Microbiology 45: 1709–1721
Biddanda, BM, Ogdahl, M, Cotner, J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46: 730–739
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: 115–122
Currie, DJ, Kalff, J (1984) A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus. Limnol Oceanogr 29: 298–310
del Giorgio, PA, Cole, JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29: 503–541
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: 3701–3709
Elser, JJ, Sterner, RW, Gorokhova, E (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3: 540–550
Fagerbakke, KM, Heldal, M, Norland, S (1996) Content of carbon, nitrogen, oxygen, sulphur and phosphorus in native and cultured bacteria. Aquat Microb Ecol 10: 15–27
Granéli, W, Bertilsson, S, Philibert, A (2004) Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquat Sci 66: 430–439
Jansson, M (1993) Uptake, exchange and excretion of orthophosphate in phosphate-starved Scenedesmus quadricauda and Pseudomonas K7. Limnol Oceanogr 38: 1162–1178
Jansson, M, Karlsson, J, Blomqvist, P (2003) Allochthonous organic carbon decreases pelagic energy mobilization in lakes. Limnol Oceanogr 48: 1711–1716
Karlsson, J, Jansson, M, Jonsson, A (2002) Similar relationships between pelagic primary and bacterial production in clearwater and humic lakes. Ecology 83: 2902–2910
Khosmanesh, A, Hart, BT, Duncand, A, Becket, R (2002) Luxury uptake of phosphorus by sediment bacteria. Water Res 36: 774–778
Lennon, JT, Pfaff, LE (2005) Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquat Microb Ecol 39: 107–119
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: 33–41
Neijssel, OM, Tempest, DW (1976) Bioenergetic aspects of aerobic growth of Klebsiells aerogenes NCTC in carbon-limited and carbon-sufficient culture. Arch Microbiol 107: 215–221
Russel, JB, Cook, GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59: 48–62
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: 1627–1631
Simon, M, Azam, F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201–213
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: 107–114
Smith, EM, Prairie, YT (2004) Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol Oceanogr 49: 137–147
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: 663–683
Tempest, DW, Neijssel, OM (1978) Eco-physiological aspects of microbial growth in aerobic nutrient limited environments. Adv Microb Ecol 2: 105–153
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 115–167
Vitousek, P (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119: 553–572
Wang, L, Miller, TD, Priscu, JC (1992) Bacterioplankton nutrient deficiency in a eutrophic lake. Arch Hydrobiol 125: 423–439
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: 2965–2971
Vrede, K (1996) Regulation of bacterioplankton production and biomass in an oligotrophic clearwater lake—the importance of the phytoplankton community. J Plankton Res 18: 1009–1032
Vrede, K (2005) Nutrient and temperature limitation of bacterioplankton growth in temperate lakes. Microb Ecol 49: 245–256
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This study was financially supported by the Swedish Research Council. We thank Ulf Westerlund for excellent assistance in the field and in the laboratory.
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Jansson, M., Bergström, AK., Lymer, D. et al. Bacterioplankton Growth and Nutrient Use Efficiencies Under Variable Organic Carbon and Inorganic Phosphorus Ratios. Microb Ecol 52, 358–364 (2006). https://doi.org/10.1007/s00248-006-9013-4
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DOI: https://doi.org/10.1007/s00248-006-9013-4