Emergence of metabolic coupling to the heterotroph Alteromonas promotes dark survival in Prochlorococcus

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