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 cocultures 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 the exudate released by Prochlorococcus or if a proxy organic carbon source was provided. Genetic analysis of Alteromonas suggested that it outcompetes Synechococcus for nitrate and/or nitrite, during which cocultured 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 nutrient-limited regions of the ocean.