Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by Crocosphaera watsonii

Crocosphaera is a major dinitrogen (N₂)-fixing microorganism, providing bioavailable nitrogen (N) to marine ecosystems. The N₂-fixing enzyme nitrogenase is deactivated by oxygen (O₂), which is abundant in marine environments. Using a cellular scale model of Crocosphaera sp. and laboratory data, we quantify the role of three O₂ management strategies by Crocosphaera sp.: size adjustment, reduced O₂ diffusivity, and respiratory protection. Our model predicts that Crocosphaera cells increase their size under high O₂ Using transmission electron microscopy, we show that starch granules and thylakoid membranes are located near the cytoplasmic membranes, forming a barrier for O₂ The model indicates a critical role for respiration in protecting the rate of N₂ fixation. Moreover, the rise in respiration rates and the decline in ambient O₂ with temperature strengthen this mechanism in warmer water, providing a physiological rationale for the observed niche of Crocosphaera at temperatures exceeding 20°C. Our new measurements of the sensitivity to light intensity show that the rate of N₂ fixation reaches saturation at a lower light intensity (∼100 μmol m^-2 s^-1) than photosynthesis and that both are similarly inhibited by light intensities of >500 μmol m^-2 s^-1 This suggests an explanation for the maximum population of Crocosphaera occurring slightly below the ocean surface.IMPORTANCECrocosphaera is one of the major N₂-fixing microorganisms in the open ocean. On a global scale, the process of N₂ fixation is important in balancing the N budget, but the factors governing the rate of N₂ fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O₂ and physical factors such as temperature and light affect N₂ fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O₂ to protect the O₂-sensitive N₂-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N₂ fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.