Quantification of the coupled dynamics of marine microbes and reactive oxygen species in laboratory batch culture...

Prochlorococcus, the smallest and most numerous phytoplankter of the oligotrophic surface ocean, is vulnerable to damage by the reactive oxygen species hydrogen peroxide (H₂O₂). The most harmful effects of exogenous H₂O₂ are mitigated by detoxifying organisms, but even at low concentrations, the ecological and biogeochemical consequences of H₂O₂ damage are not fully understood. Here, we present coupled ordinary differential equation models of the dynamics of diverse marine microbes grown in different levels of H₂O₂. We fit our model to monoculture time-series data of peroxide-sensitive Prochlorococcus and peroxide-resistant Synechococcus, picoeukaryotes, and bacteria. Our fits provide estimates of H₂O₂ cell damage and detoxification rates in these ecologically important microbes. We find significant variation in rates of cell death and H₂O₂ detoxification by taxonomy and H₂O₂ concentration. Picoplankton (Micromonas spp. or Ostreococcus spp.) and other previously investigated heterotroph helpers (Alteromonas) appear to upregulate detoxification when H₂O₂ is elevated, whereas Synechococcus detoxification rate does not vary with hydrogen peroxide concentration. As expected, elevated H₂O₂ is damaging to high light-adapted Prochlorococcus, but they are capable of modest detoxification when H₂O₂ concentration is relatively low. Our use of differential equation models to quantify parameters underlying microbe-H₂O₂ dynamics provides a basis for ecosystem models to explore the impact of reactive oxygen species on cell mortality of different ocean microbes and computational exploration of H₂O₂ impacts on microbial community composition.

Hydrogen peroxide produced naturally in the surface ocean is toxic to many abundant microbes that perform important ecosystem services such as carbon fixation. Much of the naturally occurring hydrogen peroxide produced in the surface ocean is detoxified by "helper" organisms. The healthy function of microbial communities may therefore depend upon the presence of different helpers. Mathematical models provide an important means to evaluate the impacts of hydrogen peroxide on ecosystem function. This study introduces a framework to evaluate the sensitivity of diverse microbes to hydrogen peroxide, in a manner that is amenable for inclusion in ecosystem models. It lays a foundation for future efforts to evaluate the impact of hydrogen peroxide on ecosystem function and microbial community composition.