Warming Iron-Limited Oceans Enhance Nitrogen Fixation and Drive Biogeographic Specialization of the Globally Important Cyanobacterium Crocosphaera

Primary productivity in the nutrient-poor subtropical ocean gyres depends on new nitrogen inputs from nitrogen fixers that convert inert dinitrogen gas into bioavailable forms. Temperature and iron (Fe) availability constrain marine nitrogen fixation, and both are changing due to anthropogenic ocean warming. We examined the physiological responses of the globally important marine nitrogen fixer, Crocosphaera watsonii across its full thermal range as a function of iron availability. At the lower end of its thermal range, from 22°C to 27°C, Crocosphaera growth, nitrogen fixation, and Nitrogen-specific Iron Use Efficiencies (N-IUEs, mol N fixed hour-1 mol Fe-1) increased with temperature. At an optimal growth temperature of 27°C, N-IUEs were 66% higher under iron-limited conditions than iron-replete conditions, indicating that low-iron availability increases metabolic efficiency. However, Crocosphaera growth and function decrease from 27°C to 32°C, temperatures that are predicted for an increasing fraction of tropical oceans in the future. Altogether, this suggests that Crocosphaera are well adapted to iron-limited, warm waters, within prescribed limits. A model incorporating these results under the IPCC RCP 8.5 warming scenario predicts that Crocosphaera N-IUEs could increase by a net 47% by 2100, particularly in higher-latitude waters. These results contrast with published responses of another dominant nitrogen fixer (Trichodesmium), with predicted N-IUEs that increase most in low-latitude, tropical waters. These models project that differing responses of Crocosphaera and Trichodesmium NIUEs to future warming of iron-limited oceans could enhance their current contributions to global marine nitrogen fixation with rates increasing by ~91% and ~22%, respectively, thereby shifting their relative importance to marine new production and also intensifying their regional divergence. Thus, interactive temperature and iron effects may profoundly transform existing paradigms of nitrogen biogeochemistry and primary productivity in open ocean regimes.