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
are considered as major evolutionary drivers of microbial life (Suttle,
2007). Yet, we lack quantitative approaches to assess their impact on the
marine ecosystem. Here, we provide quantification of active viral
infection in the bloom forming single celled phytoplankton Emiliania
huxleyi infected by the large virus EhV, using high-throughput single
molecule mRNA in situ hybridization of both virus and host transcripts. In
natural samples, viral infection reached only 25% of the population
despite synchronized bloom demise exposing co-existence of infected and
non-infected subpopulations. We prove that photosynthetically active cells
chronically release viral particles through non-lytic infection, and that
viral-induced cell lysis can occur without viral release, thus challenging
major assumptions regarding the life cycle of giant viruses. We could also
assess active infection in cell aggregates, linking viral infection and
carbon export to the deep ocean (Laber et al., 2018) and suggest a
potential host defense strategy by enrichment of infected cells in sinking
aggregates. Our approach can be applied to diverse marine microbial
systems, opening a mechanistic dimension to the study of biotic
interactions in the ocean.