Visualizing Active Viral Infection Reveals Diverse Cell Fates in Synchronized Algal Bloom Demise

Marine viruses are the most abundant biological entity in the ocean and considered as major evolutionary drivers of microbial life. Yet, we lack quantitative approaches to assess their impact on the marine ecosystem. Here, we provide the first quantification of active viral infection in single celled phytoplankton, by high-throughput subcellular visualization of both virus and host transcripts during an Emiliania huxleyi algal bloom infected by its large virus EhV. Viral infection reached only 25% of the population despite synchronized bloom demise. Using this approach coined Virocell-FISH, we show that metabolically active cells chronically release viral particles, and that viral-induced lysis does not systematically induce virion increase, thus challenging major assumptions regarding giant lytic viruses life cycle. We could also assess viral infection in cell aggregates, linking viruses to carbon export to the deep ocean. Our approach can be applied to diverse marine microbial systems, opening a mechanistic dimension to the study of host-pathogen interactions in the ocean.