RNA virus-mediated metabolic reprogramming in a bloom-forming, marine diatom

Abstract

Diatoms are a widespread group of phytoplankton that disproportionately influence the global carbon cycle through substantial contributions to primary production and carbon export in the ocean. Marine viruses are major drivers of host metabolic reprogramming and mortality and it is increasingly clear that RNA viruses, which primarily infect eukaryotes, are abundant and distributed throughout the global ocean. Using an integrated, multi-omics approach, we characterized the molecular and metabolic response of the model, bloom-forming, centric diatom Chaetoceros tenuissimus to RNA virus infection. Time-resolved transcriptomics revealed coordinated, differential regulation of more than a third of host genes prior to host lysis, eliciting a cascade of metabolic responses that included early shifts in sulfur and lipid metabolism, induction of nitrogen assimilation pathways, and late-stage activation of stress, signaling and death-related genes. Lipidomics revealed substantial cellular enrichment of phosphatidylethanolamine, ceramide and triacylglycerol during RNA virus infection, as well as an infection-specific shift in fatty acid composition. Collectively, these findings provide insight into the intracellular requirements for RNA virus replication and illustrate a fundamental shift in resource partitioning in infected diatoms, advancing our understanding of how RNA virus infection transforms diatom host metabolic function and downstream ecosystem dynamics.