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

Abstract

Prochlorococcus is the most numerically abundant photosynthetic organism in the oligotrophic ocean yet 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 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.