Coexistence of Photosynthetic Marine Microorganisms, Viruses, and Grazers: Toward Integration in Ocean Ecosystem Models

Photosynthetic microorganisms are responsible for primary production at the base of the marine food web that shapes ocean biogeochemistry and ecology. The growth of these microorganisms is balanced by mortality, including top-down losses by microbial grazing by heterotrophic nanoflagellates and zooplankton and infection and lysis by viruses. Notably, multiple types of grazers and viruses often coexist despite apparent competition for the same (or similar) microorganisms. Here, we develop a community model of photosynthetic microorganisms, grazers, and viruses that accounts for molar cell and virion quotas suitable for incorporation into ocean ecosystem models. Our aim is to investigate mechanisms that enable coexistence of a virus and a grazer with a single phytoplankton type. To do so, we evaluate the extent to which coexistence is facilitated by: (i) the inclusion of an infected class of the phytoplankton, potentially subject to intraguild predation, where grazers feed on virally infected microorganisms; (ii) heterogeneity in susceptibility to infection, where microorganisms vary in their resistance to the virus either intracellularly or extracellularly; and (iii) the inclusion of higher-order mortality terms for the predators. When adding an infected class, we find evidence for a trade-off between the virus latent period and virulence in facilitating a coexistence regime. The inclusion of an explicit latent period can generate oscillations of all populations that facilitate coexistence by reducing the fitness of the free virus, or lead to system collapse when oscillations become too large. Heterogeneity in phage susceptibility promotes coexistence through resource partitioning between the predators, while quadratic mortality terms widen the coexistence regime by stabilizing the system. We observe strong sensitivity of the models’ outcomes to the viral life history traits, including shifts in infected cell percentages and the balance between virally and zooplankton-induced mortality. Finally, taking advantage of algebraic calculation of model equilibria, we identify life history trait parameter combinations that yield realistic ecological properties in simplified oligotrophic and mesotrophic epipelagic environments. Importantly, our ecological models suggest that ongoing efforts to embed virus dynamics in large-scale ocean ecosystem models should include phytoplankton types that are moderately to strongly resistant to viral infection and lysis.