On the role of oxygen for nitrogen fixation in the marine cyanobacterium Trichodesmium sp.

The marine, non-heterocystous, filamentous cyanobacterium Trichodesmium shows a distinct diurnal pattern of nitrogenase activity. In an attempt to reveal the factors that control this pattern, a series of measurements were carried out using online acetylene reduction assay. Light response curves of nitrogenase were recorded applying various concentrations of oxygen. The effect of oxygen depended on the irradiance applied. Above a photon irradiance of 16 mumol m(-2) s(-1) nitrogenase activity was highest under anoxic conditions. Below this irradiance the presence of oxygen was required to achieve highest nitrogenase activity and in the dark 5% oxygen was optimal. At any oxygen concentration a photon irradiance of 100 mumol m(-2) s(-1) was saturating. When Trichodesmium was incubated in the dark, nitrogenase activity gradually decreased and this decline was higher at higher levels of oxygen. The activity recovered when the cells were subsequently incubated in the light. This recovery depended on oxygenic photosynthesis because it did not occur in the presence of DCMU [3-(3,4-dichlorophenyl)-1,1-dimethylurea]. Recovery of nitrogenase activity in the light was faster at low oxygen concentrations. The results showed that under aerobic conditions nitrogenase activity was limited by the availability of reducing equivalents suggesting a competition for electrons between nitrogenase and respiration.

[1]  J. Gallon Reconciling the incompatible: N2 fixation And O2 , 2006 .

[2]  D. Capone Marine nitrogen fixation: what's the fuss? , 2001, Current opinion in microbiology.

[3]  Fei-xue Fu,et al.  Factors affecting N fixation by the cyanobacterium Trichodesmium sp. GBRTRLI101. , 2003, FEMS microbiology ecology.

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

[5]  David M. Karl,et al.  Dinitrogen fixation in the world's oceans , 2002 .

[6]  I. Berman‐Frank,et al.  Traffic Lights in Trichodesmium. Regulation of Photosynthesis for Nitrogen Fixation Studied by Chlorophyll Fluorescence Kinetic Microscopy1 , 2004, Plant Physiology.

[7]  H. Paerl,et al.  Growth, Nitrogen Fixation, and Spectral Attenuation in Cultivated Trichodesmium Species , 1993, Applied and environmental microbiology.

[8]  E. Carpenter,et al.  New perspectives on nitrogen-fixing microorganisms in tropical and subtropical oceans. , 2000, Trends in microbiology.

[9]  Ricardo M Letelier,et al.  TRICHODESMIUM SPP. PHYSIOLOGY AND NUTRIENT FLUXES IN THE NORTH PACIFIC SUBTROPICAL GYRE , 1998 .

[10]  L. Stal,et al.  Nitrogenase activity in cyanobacteria measured by the acetylene reduction assay: a comparison between batch incubation and on-line monitoring. , 2001, Environmental microbiology.

[11]  B. Bergman,et al.  Diurnal expression of hetR and diazocyte development in the filamentous non-heterocystous cyanobacterium Trichodesmium erythraeum. , 2003, Microbiology.

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

[13]  J. Zehr,et al.  Expression of photosynthesis genes in relation to nitrogen fixation in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101 , 1999, Plant Molecular Biology.

[14]  D. Capone,et al.  Modification of the Fe Protein of Nitrogenase in Natural Populations of Trichodesmium thiebautii , 1993, Applied and environmental microbiology.

[15]  Carpenter,et al.  The marine planktonic cyanobacteria Trichodesmium spp.: photosynthetic rate measurements in the SW Atlantic Ocean , 1995 .

[16]  Y. Fujita,et al.  Regulation of nitrogenase activity in relation to the light-dark regime in the filamentous non-heterocystous cyanobacterium Trichodesmium sp. NIBB 1067 , 1992 .

[17]  P. Herman,et al.  Comparison of Models Describing Light Dependence of N2 Fixation in Heterocystous Cyanobacteria , 2002, Applied and Environmental Microbiology.

[18]  T. Kana Rapid oxygen cycling in Trichodesmium thiebautii , 1993 .

[19]  E. Carpenter,et al.  Basis for Diel Variation in Nitrogenase Activity in the Marine Planktonic Cyanobacterium Trichodesmium thiebautii , 1990, Applied and environmental microbiology.

[20]  S. Rabouille,et al.  Modeling the Dynamic Regulation of Nitrogen Fixation in the Cyanobacterium Trichodesmium sp , 2006, Applied and Environmental Microbiology.

[21]  F. Cipriano,et al.  N2 Fixation by Unicellular Bacterioplankton from the Atlantic and Pacific Oceans: Phylogeny and In Situ Rates , 2004, Applied and Environmental Microbiology.

[22]  B. Bergman,et al.  Nitrogenase quantity varies diurnally in a subset of cells within colonies of the non-heterocystous cyanobacteria Trichodesmium spp. , 1995 .

[23]  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 .

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

[25]  L. Stal,et al.  Effects of O 2 on N 2 fixation in heterocystous cyanobacteria from the Baltic Sea , 2003 .

[26]  J. Gallon,et al.  N2 Fixation by non-heterocystous cyanobacteria , 1997 .

[27]  S. Scherer,et al.  Respiration, cyanide‐insensitive oxygen uptake and oxidative phosphorylation in cyanobacteria , 1988 .

[28]  J. Gallon,et al.  Maximum rates of N2 fixation and primary production are out of phase in a developing cyanobacterial bloom in the Baltic Sea , 2002 .

[29]  P. Falkowski,et al.  Segregation of Nitrogen Fixation and Oxygenic Photosynthesis in the Marine Cyanobacterium Trichodesmium , 2001, Science.