Virus-grazer interplay enhances virus production, particle aggregation, and trophic efficiency during infection of Prochlorococcus

Viruses and grazers are fundamental agents of mortality in the oceans, impacting phytoplankton populations and organic matter cycling. Although viruses and grazers co-occur in nature, they are typically studied in isolation in laboratory experiments, limiting our understanding of their combined ecosystem impacts. Here, using a simplified ecosystem approach, we investigated individual and combined effects of the T7-like cyanopodovirus, P-SSP7, and the protistan grazer, Paraphysomonas bandaiensis, on the abundant marine cyanobacterium, Prochlorococcus MED4, and co-occurring non-photosynthetic heterotrophic bacteria (bacteria from here on). We observed that, individually, viruses and grazers caused substantial Prochlorococcus mortality. Viral lysis also triggered increases in damaged Prochlorococcus cells, dissolved organic matter release, and bacterial growth, while grazing reduced bacterial abundances. When grazers and viruses were combined, Prochlorococcus mortality was lower than expected from the sum of their individual effects. Contrary to expectations, this reduced Prochlorococcus mortality did not result in fewer viruses or grazers. Instead, virus-grazer-Prochlorococcus interplay resulted in greater virus production, maintenance of grazer growth, and a dramatic increase in particle aggregation. Our results reveal trophic cooperation and efficiency in which competition between viruses and grazers was likely mitigated, with virus progeny production enhanced by grazers, and grazer growth sustained through a shift to alternative food sources (bacteria, damaged cells, aggregates) secondarily derived from Prochlorococcus following viral lysis. The synergistic enhancement of particle aggregation via grazer-virus-phytoplankton interplay observed with the small buoyant Prochlorococcus phytoplankter underscores the importance of food web interactions for the flow of phytoplankton-fixed carbon within, and export from, the photic zone.

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