Nitrogen Fixation and Temperature Physiological Constraints on the Global Distribution of Trichodesmium – Effect of Temperature on Diazotrophy Nitrogen Fixation and Temperature

Abstract. The cyanobacterium Trichodesmium is an important link in the global nitrogen cycle due to its significant input of atmospheric nitrogen to the ocean. Attempts to incorporate Trichodesmium in ocean biogeochemical circulation models have, so far, relied on the observed correlation between temperature and Trichodesmium abundance. This correlation may result in part from a direct effect of temperature on Trichodesmium growth rates through the control of cellular biochemical processes, or indirectly through temperature influence on mixed layer depth, light and nutrient regimes. Here we present results indicating that the observed correlation of Trichodesmium with temperature in the field reflects primarily the direct physiological effects of temperature on diazotrophic growth of Trichodesmium. Trichodesmium IMS-101 (an isolate of Trichodesmium) could acclimate and grow at temperatures ranging from 20 to 34°C. Maximum growth rates (μmax=0.25 day–1) and maximum nitrogen fixation rates (0.13 mmol N mol POC−1 h–1) were measured within 24 to 30°C. Combining this empirical relationship with global warming scenarios derived from state-of-the-art climate models sets a physiological constraint on the future distribution of Trichodesmium that could significantly affect the future nitrogen input into oligotrophic waters by this diazotroph.

[1]  K. D. Pandey,et al.  Cyanobacteria in Antarctica: ecology, physiology and cold adaptation. , 2004, Cellular and molecular biology.

[2]  L. Stal,et al.  Temperature excludes N2-fixing heterocystous cyanobacteria in the tropical oceans , 2003, Nature.

[3]  P. Falkowski,et al.  Aquatic Photosynthesis: Second Edition , 1997 .

[4]  D. Capone,et al.  Stoichiometry of nitrogen and carbon utilization in cultured populations of Trichodesmium IMS101: Implications for growth , 2001 .

[5]  C. Fraser,et al.  The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Nicholas R. Bates,et al.  Modeling the effect of nitrogen fixation on carbon and nitrogen fluxes at BATS , 2001 .

[7]  J. Zehr,et al.  Circadian Rhythm of Nitrogenase Gene Expression in the Diazotrophic Filamentous Nonheterocystous CyanobacteriumTrichodesmium sp. Strain IMS 101 , 1998, Journal of bacteriology.

[8]  S. Doney,et al.  Modelling regional responses by marine pelagic ecosystems to global climate change , 2002 .

[9]  J. Sharp.  Improved analysis for “particulate” organic carbon and nitrogen from seawater1 , 1974 .

[10]  D. Scanlan,et al.  PCR Analysis of the Distribution of Unicellular Cyanobacterial Diazotrophs in the Arabian Sea , 2004, Applied and Environmental Microbiology.

[11]  N. Welschmeyer.  Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments , 1994 .

[12]  J. LaRoche,et al.  Diazotrophic Diversity and Distribution in the Tropical and Subtropical Atlantic Ocean , 2005, Applied and Environmental Microbiology.

[13]  J. Montoya,et al.  High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean , 2004, Nature.

[14]  Michael E. Salvucci,et al.  Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. , 2004, Physiologia plantarum.

[15]  J. LaRoche,et al.  The Bunsen gas solubility coefficient of ethylene as a function of temperature and salinity and its importance for nitrogen fixation assays , 2004 .

[16]  K. Fennel,et al.  A deterministic model for N2 fixation at stn. ALOHA in the subtropical North Pacific Ocean , 2001 .

[17]  E. Carpenter,et al.  Nitrogen fixation by marine Cyanobacteria: historical and global perspectives , 1999 .

[18]  E. Carpenter,et al.  Biomass and primary productivity of the cyanobacterium Trichodesmium spp. in the tropical N Atlantic ocean , 2004 .

[19]  Edward J. Carpenter,et al.  Trichodesmium, a Globally Significant Marine Cyanobacterium , 1997 .

[20]  Nicolas Gruber,et al.  Global patterns of marine nitrogen fixation and denitrification , 1997 .

[21]  J. Zehr,et al.  GROWTH AND NITROGEN FIXATION OF THE DIAZOTROPHIC FILAMENTOUS NONHETEROCYSTOUS CYANOBACTERIUM TRICHODESMIUM SP. IMS 101 IN DEFINED MEDIA: EVIDENCE FOR A CIRCADIAN RHYTHM 1 , 1996 .

[22]  M. Salvucci,et al.  Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Ricardo M Letelier,et al.  Role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean , 1996 .

[24]  Katja Fennela,et al.  A deterministic model for N 2 fixation at stn . ALOHA in the subtropical North Pacific Ocean , 2001 .

[25]  L. Stal,et al.  Variable selection pressures across lineages in Trichodesmium and related cyanobacteria based on the heterocyst differentiation protein gene hetR. , 2005, Gene.

[26]  R. Geider,et al.  Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis , 2002 .

[27]  Timothy P. Boyer,et al.  World Ocean Atlas 1994. Volume 4. Temperature , 1994 .

[28]  Julie LaRoche,et al.  Importance of the diazotrophs as a source of new nitrogen in the ocean , 2005 .

[29]  E. Carpenter,et al.  An extensive bloom of the N2-fixing cyanobacterium Trichodesmium erythraeum in the central Arabian Sea , 1998 .

[30]  T. Kana,et al.  Dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient-limitation and temperature , 1997 .

[31]  Ricardo M Letelier,et al.  The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean , 1997, Nature.

[32]  U. Schreiber,et al.  Computer-Controlled Phytoplankton Analyzer Based on a 4-Wavelengths Pam Chlorophyll Fluorometer , 1995 .

[33]  A. Ivanov,et al.  Stoichiometry of the Photosynthetic Apparatus and Phycobilisome Structure of the Cyanobacterium Plectonema boryanum UTEX 485 Are Regulated by Both Light and Temperature1 , 2002, Plant Physiology.

[34]  E. Carpenter,et al.  Growth kinetics of marine unicellular N2-fixing cyanobacterial isolates in continuous culture in relation to phosphorus and temperature , 2005 .

[35]  D. Capone,et al.  Modeling the distribution of Trichodesmium and nitrogen fixation in the Atlantic Ocean , 2004 .

[36]  Keith W. Dixon,et al.  Review of simulations of climate variability and change with the GFDL R30 coupled climate model , 2002 .

[37]  F. Lipschultz,et al.  An assessment of nitrogen fixation as a source of nitrogen to the North Atlantic Ocean , 1996 .

[38]  Houng-Yung Chen,et al.  Distribution and downward flux of Trichodesmium in the South China Sea as influenced by the transport from the Kuroshio Current , 2003 .

[39]  R. A. Olsen,et al.  The Influence of Abiotic Factors on Biological Nitrogen Fixation in Different Types of Vegetation in the High Arctic, Svalbard , 2002 .

[40]  B. Bergman,et al.  Trichodesmium in coastal waters of Tanzania: diversity, seasonality, nitrogen and carbon fixation , 2002, Hydrobiologia.

[41]  M. Salvucci,et al.  Relationship between the Heat Tolerance of Photosynthesis and the Thermal Stability of Rubisco Activase in Plants from Contrasting Thermal Environments1 , 2004, Plant Physiology.

[42]  John F. B. Mitchell,et al.  The simulation of SST, sea ice extents and ocean heat transports in a version of the Hadley Centre coupled model without flux adjustments , 2000 .

[43]  W. Koeve,et al.  Determination of particulate organic carbon and nitrogen , 2007 .

[44]  J. Montoya,et al.  A Simple, High-Precision, High-Sensitivity Tracer Assay for N(inf2) Fixation , 1996, Applied and environmental microbiology.