Haptophyte-infecting viruses change the genome condensing proteins of dinoflagellates

Giant viruses are extraordinary members of the virosphere due to their structural complexity and high diversity in gene content. Haptophytes are ecologically important primary producers in the ocean, and all known viruses that infect haptophytes are giant viruses. However, little is known about the specifics of their infection cycles and the responses they trigger in their host cells. Our in-depth electron microscopic, phylogenomic and virion proteomic analyses of two haptophyte-infecting giant viruses, Haptolina ericina virus RF02 (HeV RF02) and Prymnesium kappa virus RF02 (PkV RF02), unravel their large capacity for host manipulation and arsenals that function during the infection cycle from virus entry to release. The virus infection induces significant morphological changes in the host cell that is manipulated to build a virus proliferation factory. Both viruses' genomes encode a putative nucleoprotein (dinoflagellate/viral nucleoprotein; DVNP), which was also found in the virion proteome of PkV RF02. Phylogenetic analysis suggests that DVNPs are widespread in marine giant metaviromes. Furthermore, the analysis shows that the dinoflagellate homologues were possibly acquired from viruses of the order Imitervirales. These findings enhance our understanding of how viruses impact the biology of microalgae, providing insights into evolutionary biology, ecosystem dynamics, and nutrient cycling in the ocean.