Prochlorococcus exudate stimulates heterotrophic bacterial competition with rival phytoplankton for available nitrogen

The marine cyanobacterium Prochlorococcus numerically dominates the phytoplankton community of the nutrient-limited open ocean, establishing itself as the most abundant photosynthetic organism on Earth. This ecological success has been attributed to lower cell quotas for limiting nutrients, superior resource acquisition, and other advantages associated with cell size reduction and genome streamlining. In this study we tested the prediction that Prochlorococcus outcompetes its rivals for scarce nutrients, and that this advantage leads to its numerical success in nutrient-limited waters. Strains of Prochlorococcus and its sister genus Synechococcus grew well in both mono- and co-culture when nutrients were replete. However, in nitrogen-limited medium Prochlorococcus outgrew Synechococcus, but only when heterotrophic bacteria were also present. In the nitrogen-limited medium, the heterotroph Alteromonas macleodii outcompeted Synechococcus for nitrogen, but only if stimulated by exudate released by Prochlorococcus, or if a proxy organic carbon source was provided. Analysis of a nitrate reductase mutant Alteromonas suggested that Alteromonas outcompetes Synechococcus for nitrate, during which co-cultured Prochlorococcus grows on ammonia or other available nitrogen species. We propose that Prochlorococcus can stimulate antagonism between heterotrophic bacteria and potential phytoplankton competitors through a metabolic cross-feeding interaction, and this stimulation could contribute to the numerical success of Prochlorococcus in the nutrient-limited regions of the ocean. Significance StatementIn nutrient-poor habitats, the competition for limited resources is thought to select for organisms with enhanced ability to scavenge nutrients and utilize them efficiently. Such adaptations characterize the cyanobacterium Prochlorococcus, the most abundant photosynthetic organism in the nutrient-limited open ocean. In this study the competitive superiority of Prochlorococcus over a rival cyanobacterium, Synechococcus, was captured in laboratory culture. Critically, this outcome was achieved only when key aspects of the open ocean were simulated: a limited supply of nitrogen, and the presence of heterotrophic bacteria. Results indicate that Prochlorococcus promotes its numerical dominance over Synechococcus by energizing the heterotrophs ability to outcompete Synechococcus for available nitrogen. This study demonstrates how interactions between trophic groups can influence interactions within trophic groups.