Predicting how O2 characterizes the niche of marine unicellular diazotroph Crocosphaera

Crocosphaera is a major marine unicellular nitrogen fixer, providing bioavailable nitrogen essential to marine ecosystem productivity. A major energetic cost of N₂ fixation stems from the need to maintain low intracellular O₂, in surface ocean habitats where O₂ is abundant, yet these costs are poorly understood. We present a mechanistic model of cellular metabolisms (Cell Flux Model) resolving C, N and O₂ fluxes to show how the energetic costs of O₂ management constrain their ecological niche and biogeographic distribution. The model shows that Crocosphaera combines multiple strategies to manage intracellular O₂: respiratory protection, size adjustment, and low diffusivity membranes. Even with this combination of strategies, the level of respiratory protection is only sufficient at high temperature, explaining why the geographic range of Crocosphaera is limited to waters warmer than 20 ºC. Since the respiratory protection is costly in C, management of O₂ requires high rates of photosynthesis, constraining the depths with sufficient light for Crocosphaera. However, we show that such C cost can be reduced by the formation of cell colonies with a division of metabolic roles in which only a fraction of cells fix nitrogen with respiratory protection. These quantified niche constraints provide useful implication in predicting hot spots of nitrogen fixation in the oligotrophic ocean.