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Nutrient Constraints on Metabolism Affect the Temperature Regulation of Aquatic Bacterial Growth Efficiency

  • Microbiology of Aquatic Systems
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Abstract

Inorganic nutrient availability and temperature are recognized as major regulators of organic carbon processing by aquatic bacteria, but little is known about how these two factors interact to control bacterial metabolic processes. We manipulated the temperature of boreal humic stream water samples within 0–25°C and measured bacterial production (BP) and respiration (BR) with and without inorganic nitrogen + phosphorus addition. Both BP and BR increased exponentially with temperature in all experiments, with Q 10 values varying between 1.2 and 2.4. The bacterial growth efficiency (BGE) showed strong negative relationships with temperature in nutrient-enriched samples and in natural stream water where community-level BP and BR were not limited by nutrients. However, there were no relationships between BGE and temperature in samples where BP and BR were significantly constrained by the inorganic nutrient availability. The results suggest that metabolic responses of aquatic bacterial communities to temperature variations can be strongly dependent on whether the bacterial metabolism is limited by inorganic nutrients or not. Such responses can have consequences for both the carbon flux through aquatic food webs and for the flux of CO2 from aquatic systems to the atmosphere.

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References

  1. Azam F, Fenchel T, Field JG, Meyer-Reil RA, Thingstad TF (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  2. Jones RI (1992) The influence of humic substances on lacustrine planktonic food-chains. Hydrobiologia 229:73–91

    CAS  Google Scholar 

  3. Jansson M, Persson L, DeRoos AM, Jones RI, Tranvik LJ (2007) Terrestrial carbon and intraspecific size-variation shape lake ecosystems. Trends Ecol Evol 22:316–322

    Article  PubMed  Google Scholar 

  4. del Giorgio PA, Cole JJ, Cimbleris A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385:148–151

    Article  Google Scholar 

  5. Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10:171–184

    Article  CAS  Google Scholar 

  6. del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541

    Article  Google Scholar 

  7. Nedwell DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101–111

    Article  CAS  PubMed  Google Scholar 

  8. Quinlan AV (1981) The thermal sensitivity of generic Michaelis–Menten processes without catalyst denaturation or inhibition. J Therm Biol 6:103–114

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  10. Apple JK, del Giorgio PA, Kemp WM (2006) Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquat Microb Ecol 43:243–254

    Article  Google Scholar 

  11. Hall EK, Cotner JB (2007) Interactive effect of temperature and resources on carbon cycling by freshwater bacterioplankton communities. Aquat Microb Ecol 49:35–45

    Article  Google Scholar 

  12. Hall EK, Neuhauser C, Cotner JB (2008) Toward a mechanistic understanding of how natural bacterial communities respond to changes in temperature in aquatic ecosystems. ISME J 2:471–481

    Article  CAS  PubMed  Google Scholar 

  13. Rivkin RB, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400

    Article  CAS  PubMed  Google Scholar 

  14. Lambers H, Chapin FS, Pons TL (1998) Plant physiological ecology. Springer, Berlin

    Google Scholar 

  15. Sand-Jensen K, Pedersen NL, Søndergaard M (2007) Bacterial metabolism in small temperate streams under contemporary and future climates. Freshw Biol 52:2340–2353

    Article  Google Scholar 

  16. Lopez-Urrutia A, Moran XAG (2007) Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling. Ecology 88:817–822

    Article  PubMed  Google Scholar 

  17. Jansson M (1998) Nutrient limitation and bacteria–phytoplankton interactions in humic lakes. In: Tranvik LJ, Hessen DO (eds) Aquatic humic substances: ecology and biogeochemistry. Springer, Berlin, pp 177–196

    Google Scholar 

  18. Vadstein O (2000) Heterotrophic, planktonic bacteria and cycling of phosphorus—phosphorus requirements, competitive ability, and food web interactions. Adv Microb Ecol, vol. 16. Kluwer/Plenum, New York, pp. 115–167

  19. Hessen DO, Anderson TR (2008) Excess carbon in aquatic organisms and ecosystems: physiological, ecological, and evolutionary implications. Limnol Oceanogr 53:1685–1696

    CAS  Google Scholar 

  20. Jansson M, Bergström AK, Lymer D, Vrede K, Karlsson J (2006) Bacterioplankton growth and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microb Ecol 52:358–364

    Article  CAS  PubMed  Google Scholar 

  21. Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K, Fortino K, Knoll LB, Kortelainen PL, Kutser T, Larsen S, Laurion I, Leech DM, McCallister SL, McKnight DM, Melack JM, Overholt E, Porter JA, Prairie Y, Renwick WH, Roland F, Sherman BS, Schindler DW, Sobek S, Tremblay A, Vanni MJ, Verschoor AM, von Wachenfeldt E, Weyhenmeyer GA (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54:2298–2314

    CAS  Google Scholar 

  22. Nilsson M, Sagerfors J, Buffam I, Laudon H, Eriksson T, Grelle A, Klemedtsson L, Weslien P, Lindroth A (2008) Contemporary carbon accumulation in a boreal oligotrophic minerogenic mire—a significant sink after accounting for all C-fluxes. Glob Chang Biol 14:2317–2332

    Article  Google Scholar 

  23. Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochem Cycles 23:GB2023

    Article  Google Scholar 

  24. Apps MJ, Kurz WA, Luxmoore RJ, Nilsson LO, Sedjo RA, Schmidt R, Simpson LG, Vinson TS (1993) Boreal forests and tundra. Water Air Soil Poll 70:39–53

    Article  CAS  Google Scholar 

  25. Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436

    Article  Google Scholar 

  26. Wetzel RG (2001) Limnology: lake and river ecosystems. Academic, San Diego

    Google Scholar 

  27. Buffam I, Laudon H, Temnerud J, Mörth CM, Bishop K (2007) Landscape-scale variability of acidity and dissolved organic carbon during spring flood in a boreal stream network. J Geophys Res Biogeosci 112:G01022

    Article  Google Scholar 

  28. Berggren M, Laudon H, Jansson M (2007) Landscape regulation of bacterial growth efficiency in boreal freshwaters. Global Biogeochem Cycles 21:GB4002

    Article  Google Scholar 

  29. Berggren M, Laudon H, Haei M, Ström L, Jansson M (2010) Efficient aquatic bacterial metabolism of dissolved low molecular weight compounds from terrestrial sources. ISME J 4:408–416

    Article  CAS  PubMed  Google Scholar 

  30. Duckworth OW, Holmström SJM, Pena J, Sposito G (2009) Biogeochemistry of iron oxidation in a circumneutral freshwater habitat. Chem Geol 260:149–158

    Article  CAS  Google Scholar 

  31. Bergström AK, Jansson M (2000) Bacterioplankton production in humic Lake Örtrasket in relation to input of bacterial cells and input of allochthonous organic carbon. Microb Ecol 39:101–115

    Article  PubMed  Google Scholar 

  32. Lindström ES, Forslund M, Algesten G, Bergström AK (2006) External control of bacterial community structure in lakes. Limnol Oceanogr 51:339–342

    Article  Google Scholar 

  33. Ågren A, Buffam I, Jansson M, Laudon H (2007) Importance of seasonality and small streams for the landscape regulation of dissolved organic carbon export. J Geophys Res Biogeosci 112:G03003

    Article  Google Scholar 

  34. Berggren M, Laudon H, Jansson M (2009) Hydrological control of organic carbon support for bacterial growth in boreal headwater streams. Microb Ecol 57:170–178

    Article  PubMed  Google Scholar 

  35. Ågren A, Berggren M, Laudon H, Jansson M (2008) Terrestrial export of highly bioavailable carbon from small boreal catchments in spring floods. Freshw Biol 53:964–972

    Article  Google Scholar 

  36. Williams PJ, del Giorgio PA (2005) Respiration in aquatic ecosystems: history and background. In: del Giorgio PA, Williams PJ (eds) Respiration in aquatic ecosystems. Oxford University Press, Oxford, pp 1–17

  37. Daniel C, Gutseit K, Anesio AM, Granéli W (2005) Microbial food webs in the dark: independence of lake plankton from recent algal production. Aquat Microb Ecol 38:113–123

    Article  Google Scholar 

  38. Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51:201–213

    Article  CAS  Google Scholar 

  39. del Giorgio PA, Gasol JM, Condon R, Longnecker K, Bouvier T, Bouvier C, Sherr E (2010) Coherent patterns in bacterial growth, growth efficiency, and leucine metabolism along a Northeast Pacific inshore–offshore transect. Limnol Oceanogr (in press)

  40. Stepanauskas R, Laudon H, Jørgensen NOG (2000) High DON bioavailability in boreal streams during a spring flood. Limnol Oceanogr 45:1298–1307

    Article  CAS  Google Scholar 

  41. Russell JB, Cook GM (1995) Energetics of bacterial growth—balance of anabolic and catabolic reactions. Microbiol Rev 59:48–62

    CAS  PubMed  Google Scholar 

  42. Hall EK, Dzialowski AR, Stoxen SM, Cotner JB (2009) The effect of temperature on the coupling between phosphorus and growth in lacustrine bacterioplankton communities. Limnol Oceanogr 54:880–889

    CAS  Google Scholar 

  43. Russell NJ, Fukunaga N (1990) A comparison of thermal adaptation of membrane-lipids in psychrophilic and thermophilic bacteria. FEMS Microbiol Rev 75:171–182

    Article  CAS  Google Scholar 

  44. Mansilla MC, Cybulski LE, Albanesi D, de Mendoza D (2004) Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol 186:6681–6688

    Article  CAS  PubMed  Google Scholar 

  45. Kritzberg ES, Arrieta JM, Duarte CM (2010) Temperature and phosphorus regulating carbon flux through bacteria in a coastal marine system. Aquat Microb Ecol 58:141–151

    Article  Google Scholar 

  46. Smith EM, del Giorgio PA (2003) Low fractions of active bacteria in natural aquatic communities? Aquat Microb Ecol 31:203–208

    Article  Google Scholar 

  47. Adams HE, Crump BC, Kling GW (2010) Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environ Microbiol 12:1319–1333

    Article  CAS  PubMed  Google Scholar 

  48. Laudon H, Köhler S, Buffam I (2004) Seasonal TOC export from seven boreal catchments in northern Sweden. Aquat Sci 66:223–230

    Article  Google Scholar 

  49. Pomeroy LR, Sheldon JE, Sheldon WM, Peters F (1995) Limits to growth and respiration of bacterioplankton in the Gulf of Mexico. Mar Ecol Prog Ser 117:259–268

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  51. Kroer N (1993) Bacterial growth efficiency on natural dissolved organic matter. Limnol Oceanogr 38:1282–1290

    Article  CAS  Google Scholar 

  52. Motegi C, Nagata T, Miki T, Weinbauer MG, Legendre L, Rassoulzadegan F (2009) Viral control of bacterial growth efficiency in marine pelagic environments. Limnol Oceanogr 54:1901–1910

    CAS  Google Scholar 

  53. Säwström C, Laybourn-Parry J, Granéli W, Anesio AM (2007) Heterotrophic bacterial and viral dynamics in Arctic freshwaters: results from a field study and nutrient-temperature manipulation experiments. Polar Biol 30:1407–1415

    Article  Google Scholar 

  54. Mathias CB, Kirschner AKT, Velimirov B (1995) Seasonal variations of virus abundance and viral control of the bacterial production in a backwater system of the Danube River. Appl Environ Microbiol 61:3734–3740

    CAS  PubMed  Google Scholar 

  55. Säwström C, Granéli W, Laybourn-Parry J, Anesio AM (2007) High viral infection rates in Antarctic and Arctic bacterioplankton. Environ Microbiol 9:250–255

    Article  PubMed  Google Scholar 

  56. Reinthaler T, van Aken H, Veth C, Aristegui J, Robinson C, Williams P, Lebaron P, Herndl GJ (2006) Prokaryotic respiration and production in the meso- and bathypelagic realm of the eastern and western North Atlantic basin. Limnol Oceanogr 51:1262–1273

    Article  CAS  Google Scholar 

  57. Pradeep Ram AS, Nishimura Y, Tomaru Y, Nagasaki K, Nagata T (2010) Seasonal variation in viral-induced mortality of bacterioplankton in the water column of a large mesotrophic lake (Lake Biwa, Japan). Aquat Microb Ecol 58:249–259

    Article  Google Scholar 

  58. Berggren M, Laudon H, Jansson M (2009) Aging of allochthonous organic carbon regulates bacterial production in unproductive boreal lakes. Limnol Oceanogr 54:1333–1342

    CAS  Google Scholar 

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Acknowledgments

The financial support for this work was provided by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) within the LEREC program and the Swedish Research Council (VR). The Knut and Alice Wallenberg Foundation provided resources for the laboratory equipment used to measure respiration. Samples for the study were collected by the Krycklan Catchment crew.

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Correspondence to Martin Berggren.

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Berggren, M., Laudon, H., Jonsson, A. et al. Nutrient Constraints on Metabolism Affect the Temperature Regulation of Aquatic Bacterial Growth Efficiency. Microb Ecol 60, 894–902 (2010). https://doi.org/10.1007/s00248-010-9751-1

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