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Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise
Flora Vincent, Uri Sheyn, Z. Porat, D. Schatz, A. Vardi
Significance Despite years of research in aquatic virology, we remain unable to estimate viral-induced mortality in the ocean and, consequently, to resolve viral impact on nutrient fluxes and microbial dynamics. Here, we assess active infection in a…
Significance Despite years of research in aquatic virology, we remain unable to estimate viral-induced mortality in the ocean and, consequently, to resolve viral impact on nutrient fluxes and microbial dynamics. Here, we assess active infection in algal single cells by subcellular visualization of virus and host transcripts, revealing the coexistence of infected and noninfected subpopulations. We revisit major assumptions of a giant virus’ life cycle: cells can produce virions without lysing and can lyse without producing virions. In a natural algal bloom, only 25% of cells were infected, highlighting the importance of other mortality agents. Enrichment of infected cells in cell aggregates suggests potential host defense strategies. Our approach opens a mechanistic dimension to the study of marine microbial interactions. Marine viruses are the most abundant biological entity in the ocean and are considered as major evolutionary drivers of microbial life [C. A. Suttle, Nat. Rev. Microbiol. 5, 801–812 (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 messenger RNA in situ hybridization (smFISH) of both virus and host transcripts. In natural samples, viral infection reached only 25% of the population despite synchronized bloom demise exposing the coexistence of infected and noninfected subpopulations. We prove that photosynthetically active cells chronically release viral particles through nonlytic 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 [C. P. Laber et al., Nat. Microbiol. 3, 537–547 (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.
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5
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5 | 2020 |
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