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

Crocosphaera is a major dinitrogen (N(2))-fixing microorganism, providing bioavailable nitrogen (N) to marine ecosystems. The N(2)-fixing enzyme nitrogenase is deactivated by oxygen (O(2)), which is abundant in marine environments. Using a cellular scale model of Crocosphaera sp. and laboratory data, we quantify the role of three O(2) management strategies by Crocosphaera sp.: size adjustment, reduced O(2) diffusivity, and respiratory protection. Our model predicts that Crocosphaera cells increase their size under high O(2). Using transmission electron microscopy, we show that starch granules and thylakoid membranes are located near the cytoplasmic membranes, forming a barrier for O(2). The model indicates a critical role for respiration in protecting the rate of N(2) fixation. Moreover, the rise in respiration rates and the decline in ambient O(2) 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 N(2) 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. IMPORTANCE Crocosphaera is one of the major N(2)-fixing microorganisms in the open ocean. On a global scale, the process of N(2) fixation is important in balancing the N budget, but the factors governing the rate of N(2) 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 O(2) and physical factors such as temperature and light affect N(2) fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O(2) to protect the O(2)-sensitive N(2)-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N(2) fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.