Resource competition modeling suggests hydrogen peroxide determines competitive outcomes among oligotrophic...

Prochlorococcus is the most numerically abundant photosynthetic organism in the oligotrophic ocean; yet, it is vulnerable to damage by the reactive oxygen species (ROS) hydrogen peroxide (H₂O₂). Detoxifying microbes and abiotic decay are thought to mitigate the most harmful impacts of H₂O₂, but the ecological impacts of ROS on ocean microbial community composition are not fully understood. Here, we introduce ROS dynamics within a resource competition model to investigate H₂O₂ impacts on a community with one catalase negative Prochlorococcus analogue, one catalase positive Synechococcus analogue, and a heterotrophic bacterium. Model parameters defining resource utilization, H₂O₂ detoxification, and H₂O₂-mediated cell death are constrained with data from laboratory experiments. With these ecologically realistic parameter values, we investigate the community composition for a range of ammonium and H₂O₂ supply rates. In the absence of a heterotrophic bacterium, Synechococcus' modest ability to detoxify H₂O₂ facilitates the survival of Prochlorococcus under conditions that would otherwise be fatal. However, in the absence of a strong bacterial detoxifier, unrealistically high Synechococcus concentrations (>10⁶ mL^-1) are required for it to coexist with Prochlorococcus on a single limiting nutrient. Coexistence among Prochlorococcus and Synechococcus at ecologically realistic cell densities and H₂O₂ concentrations is observed when heterotrophic bacteria with high detoxification rates reach cell densities on the order of 10⁵ cells mL^-1. Our analysis suggests that environmentally relevant ROS concentrations have the potential to determine whether Prochlorococcus and Synechococcus coexist on ammonium and points to the importance of ROS supply and degradation for understanding marine cyanobacteria ecology.