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Abstract Prochlorococcus is found throughout the euphotic zone in the oligotrophic open ocean. Deep mixing and sinking while attached to particles can, however, transport Prochlorococcus cells below this sunlit zone, depriving them of light for extended periods of time. Previous work has shown that Prochlorococcus by itself cannot survive extended periods of darkness. However, when co-cultured with a heterotrophic microbe and subjected to repeated periods of extended darkness, Prochlorococcus cells develop an epigenetically inherited dark-tolerant phenotype that can survive longer periods of darkness. Here we examine the metabolic and physiological changes underlying this adaptation using co-cultures of dark-tolerant and parental strains of Prochlorococcus, each grown with the heterotroph Alteromonas under diel light:dark conditions. The relative abundance of Alteromonas was higher in dark-tolerant than parental co-cultures, while dark-tolerant Prochlorococcus cells were larger, contained less chlorophyll, and were less synchronized to the light:dark cycle. Meta-transcriptome analysis revealed that dark-tolerant co-cultures undergo a joint change, in which Prochlorococcus undergoes a relative shift from photosynthesis to respiration, while Alteromonas shifts toward using more organic acids instead of sugars. Furthermore, the transcriptome data suggested enhanced biosynthesis of amino acids and purines in dark-tolerant Prochlorococcus and enhanced degradation of these compounds in Alteromonas. Collectively, our results demonstrate that dark adaptation involves a strengthening of the metabolic coupling between Prochlorococcus and Alteromonas, presumably mediated by an enhanced, and compositionally modified, carbon exchange between the two species. 

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 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 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 N-IUEs 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.