Iron nutrition and metabolism of the marine diazotrophic cyanobacterium, Trichodesmium spp

Biological nitrogen fixation by the marine cyanobacterium Trichodesmium can potentially relieve nitrogen stress to phytoplankton assemblages in vast regions of the ocean where inorganic nitrogen species are depleted. Despite the selective advantage of the de novo synthesis of biologically available nitrogen in a nitrate poor environment, Trichodesmium spp. is not uniformly abundant among oligotrophic regions. Iron has been suggested to limit both Trichodesmium biomass and biomass-specific rates of N₂ fixation, due to the high iron requirement of the nitrogenase enzyme and low oceanic iron concentrations. A semi-empirical model of the IUE of diazotrophic growth for Trichodesmium was computed from considerations of the Fe content and reaction rates of the nitrogenase complex and PSI:PSII ratios, as well as field measurements of Mehler activity, cellular Fe-superoxide dismutase activity, and diel variability in C and N₂ fixation. The range of WE values was 2900–7700 mol C·mol Fe−1·d·1, 7–17 fold lower than calculated for a phytoplankter with 1:1 PSI:II stoichiometry growing on reduced N. In cultures of Trichodesmium IMS 101, the IUE was 9-fold lower for cells growing diazotrophically versus on growth on NH₄+. The Fe quotas necessary to support a growth rate of 0.1 d−1 under diazotrophy and ammonium were 38 and 8 Fe:C (μmol:mol), respectively. This 5-fold increase in Fe demand reflects the influences of the lower IUE and the greater maintenance Fe:C requirement at zero growth rate under diazotrophy (13.5 versus 5.2 μmol:mol). Cultures were capable of acquiring Fe:C at levels of at least 500 μmol:mol; such luxury uptake is an important strategy within an environment with episodic iron inputs. The metabolic model and lab culture data yield a range of predicted intracellular Fe:C requirements for field populations of 27–48 Fe:C (μmol:mol) at a specific growth rate of 0.1 d−1. Comparison of Fe:C contents in field populations of Trichodesmium with the modeled or empirical Fe:C requirements suggests that half the populations collected off the north coast of Australia may have been iron limited, whereas most North Atlantic and Caribbean Sea populations sampled had Fe:C contents exceeding the Fe required to support the observed rates of N₂ fixation.