Mechanistic model for the coexistence of nitrogen fixation and photosynthesis in marine Trichodesmium

The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O₂) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditions that would allow Trichodesmium to carry out its two conflicting metabolic processes of N₂ fixation and photosynthesis. First, the model indicates that managing cellular O₂ to permit N₂ fixation requires high rates of respiratory O₂ consumption. The energetic cost amounts to ~80% of daily C fixation, comparable to the observed diminution of the growth rate of Trichodesmium relative to other phytoplankton. Second, by forming a trichome of connected cells, Trichodesmium can segregate N₂ fixation from photosynthesis. The transfer of stored C to N-fixing cells fuels the respiratory O₂ consumption that protects nitrogenase, while the reciprocal transfer of newly fixed N to C-fixing cells supports cellular growth. Third, despite Trichodesmium lacking the structural barrier found in heterocystous species, the model predicts low diffusivity of cell membranes, a function that may be explained by the presence of Gramnegative membrane, production of extracellular polysaccharide substances (EPS), and "buffer cells" that intervene between N₂-fixing and photosynthetic cells. Our results suggest that all three factors - respiratory protection, trichome formation, and diffusion barriers - represent essential strategies that, despite their energetic costs, facilitate the growth of Trichodesmium in the oligotrophic aerobic ocean and permit it to be a major source of new reactive nitrogen. IMPORTANCE Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a longstanding question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates that the life span of intracellular oxygen is extremely short, thus enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis.