Rival phytoplankton contribute to the cross protection of Prochlorococcus from oxidative stress

The marine cyanobacterium Prochlorococcus numerically dominates the phytoplankton communities in all lower latitude, open ocean environments. Having lost the catalase gene, Prochlorococcus is highly susceptible to exogenous hydrogen peroxide (H₂O₂) produced at the ocean's surface. Protection by H₂O₂-scavenging heterotrophic "helper" bacteria has been demonstrated in laboratory cultures and implicated as an important mechanism of Prochlorococcus survival in the ocean. Importantly, some other phytoplankton can also scavenge H₂O₂, suggesting these competing microbes may inadvertently protect Prochlorococcus. In this study, we assessed the ability of co-occurring phytoplankton, the cyanobacterium Synechococcus and picoeukaryotes Micromonas and Ostreococcus, to protect Prochlorococcus from H₂O₂ exposure when cocultured at ecologically relevant abundances. All three genera could significantly degrade H₂O₂ and diminish Prochlorococcus mortality during H₂O₂ exposures simulating photochemical production and rainfall events. We suggest that these phytoplankton groups contribute significantly to the H₂O₂ microbial sink of the open ocean, thus complicating their relationships with and perhaps contributing to the evolutionary history of Prochlorococcus.IMPORTANCEThe marine cyanobacterium Prochlorococcus is the most abundant photosynthetic organism on the planet and is crucially involved in microbial community dynamics and biogeochemical cycling in most tropical and subtropical ocean waters. This success is due, in part, to the detoxification of the reactive oxygen species hydrogen peroxide (H₂O₂) performed by "helper" organisms. Earlier work identified heterotrophic bacteria as helpers, and here, we demonstrate that rival cyanobacteria and picoeukaryotic phytoplankton can also contribute to the survival of Prochlorococcus during exposure to H₂O₂. Whereas heterotrophic bacteria helper organisms can benefit directly from promoting the survival of carbon-fixing Prochlorococcus cells, phytoplankton helpers may suffer a twofold injury: production of H₂O₂ degrading enzymes constrains already limited resources in oligotrophic environments, and the activity of these enzymes bolsters the abundance of their numerically dominant competitor. These findings build toward a better understanding of the intricate dynamics and interactions that shape microbial community structure in the open ocean.