Plankton-infecting relatives of herpesviruses clarify the evolutionary trajectory of giant viruses

DNA viruses have a major influence on the ecology and evolution of cellular organisms, but their overall diversity and evolutionary trajectories remain elusive. Here, we performed a phylogeny-guided genome-resolved metagenomic survey of the sunlit oceans which exposed a major, previously undescribed clade of large eukaryotic DNA viruses. Viruses in this clade encode a virion morphogenesis module characteristic of the realm Duplodnaviria , which until now included Caudoviricetes (tailed phages) and Herpesvirales (animal-infecting viruses). The conservation of the morphogenetic module firmly places the new clade within Duplodnaviria as a phylum-level group, which we name ‘ Mirusviricota ’. Remarkably, a larger fraction of ‘Mirusviricota’ genes, including hallmark informational markers, have homologs in giant eukaryotic DNA viruses from the realm Varidnaviria . We suggest that ‘ Mirusviricota ’ played a key role in the evolution of eukaryotic DNA viruses and provides missing links in the evolution of both animal herpesviruses from tailed prokaryotic viruses and giant varidnaviruses from smaller relatives. Our results are supported by more than 100 manually curated environmental genomes, including a near-complete contiguous genome of 432 Kbp. The prevalence of ‘ Mirusviricota ’ viruses within plankton and their classification into several phylogenetically diverse clades emphasizes their potential impact in marine ecosystems. Finally, genomic and environmental data indicate that ‘Mirusviricota’ harbor a rich, functionally diverse gene repertoire, including multiple heliorhodopsins, which modulates virus-host interactions in the sunlit oceans. Cover The environmental DNA sequencing and bioinformatics legacies of Tara Oceans and anvi’o exposed a putative new phylum dubbed “ Mirusviricota ” by means of phylogeny-guided genome-Resolved metagenomics . Unexpectedly, the mirusviruses are plankton-infecting relatives of herpesviruses that clarify the evolutionary trajectory of prominent large and giant viruses from another realm. ![Figure][1] Modified from the original planktonic illustration of Noan Le Bescot ### Competing Interest Statement The authors have declared no competing interest. [1]: pending:yes