Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling.

Our view of the effects of temperature on bacterial carbon fluxes in the ocean has been confounded by the interplay of resource availability. Using an extensive compilation of cell-specific bacterial respiration (BRi) and production (BPi), we show that both physiological rates respond to changing temperature in a similar manner and follow the predictions of the metabolic theory of ecology. Their apparently different temperature dependence under warm, oligotrophic conditions is due to strong resource limitation of BP, but not of BRi. Thus, and despite previous preconception, bacterial growth efficiency (BGE = BPi/[BPi + BRi]) is not directly regulated by temperature, but by the availability of substrates for growth. We develop simple equations that can be used for the estimation of bacterial community metabolism from temperature, chlorophyll concentration, and bacterial abundance. Since bacteria are the greatest living planktonic biomass, our results challenge current understanding of how warming and shifts in ecosystem trophic state will modify oceanic carbon cycle feedbacks to climate change.

[1]  Svante Arrhenius,et al.  Quantitative laws in biological chemistry , 2009 .

[2]  W. Kemp,et al.  Temperature Regulation of Bacterial Production, Respiration, and Growth Efficiency in a Temperate Salt-marsh Estuary , 2006 .

[3]  Xabier Irigoien,et al.  Scaling the metabolic balance of the oceans. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[4]  William K. W. Li,et al.  Coherent Sign Switching in Multiyear Trends of Microbial Plankton , 2006, Science.

[5]  P. White,et al.  The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats , 1991, Microbial Ecology.

[6]  R. Malmstrom,et al.  Control of bacterial growth by temperature and organic matter in the Western Arctic , 2005 .

[7]  Jonathan J. Cole,et al.  Temperature independence of carbon dioxide supersaturation in global lakes , 2005 .

[8]  T. Reinthaler,et al.  Relationship between Bacterioplankton Richness, Respiration, and Production in the Southern North Sea , 2005, Applied and Environmental Microbiology.

[9]  James H. Brown,et al.  Linking the global carbon cycle to individual metabolism , 2005 .

[10]  A. Schmittner.  Decline of the marine ecosystem caused by a reduction in the Atlantic overturning circulation , 2005, Nature.

[11]  P. Williams,et al.  Respiration in Aquatic Ecosystems: History and Background , 2005 .

[12]  William K. W. Li,et al.  Macroecological limits of heterotrophic bacterial abundance in the ocean , 2004 .

[13]  Scott C. Doney,et al.  Response of ocean ecosystems to climate warming , 2004 .

[14]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[15]  Evan P. Economo,et al.  Scaling metabolism from organisms to ecosystems , 2003, Nature.

[16]  Carlos M. Duarte,et al.  Respiration in the open ocean , 2002, Nature.

[17]  C. Pedrós-Alió,et al.  Dissolved Primary Production and the Strength of Phytoplankton– Bacterioplankton Coupling in Contrasting Marine Regions , 2002, Microbial Ecology.

[18]  James H. Brown,et al.  Effects of size and temperature on developmental time , 2002, Nature.

[19]  H. Hoppe,et al.  Bacterial growth and primary production along a north–south transect of the Atlantic Ocean , 2002, Nature.

[20]  James H. Brown,et al.  Effects of Size and Temperature on Metabolic Rate , 2001, Science.

[21]  L. Legendre,et al.  Biogenic carbon cycling in the upper ocean: effects of microbial respiration. , 2001, Science.

[22]  W. Wiebe,et al.  Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria , 2001 .

[23]  C. Duarte,et al.  Comparative analyses in aquatic microbial ecology: how far do they go? , 2000, FEMS microbiology ecology.

[24]  J. Cole,et al.  BACTERIAL GROWTH EFFICIENCY IN NATURAL AQUATIC SYSTEMS , 1998 .

[25]  Jonathan J. Cole,et al.  Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems , 1997, Nature.

[26]  D. Kirchman.  Microbial breathing lessons , 1997, Nature.

[27]  R. Jahnke,et al.  Quantifying the role of heterotrophic bacteria in the carbon cycle: A need for respiration rate measurements1 , 1995 .

[28]  H. Ducklow,et al.  Temperature and substrate regulation of bacterial abundance, production and specific growth rate in Chesapeake Bay, USA , 1994 .

[29]  P. Williams,et al.  Temperature and Antarctic plankton community respiration , 1993 .