Abstract 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 and discovered plankton-infecting relatives of herpesviruses that form a putative new phylum dubbed ‘ Mirusviricota ’. The virion morphogenesis module of this large monophyletic clade is typical of viruses from the realm Duplodnaviria , with the major capsid protein fold being a likely structural intermediate between the capsid proteins of Caudoviricetes (tailed phages) and Herpesvirales (animal-infecting viruses). Yet, a substantial fraction of ‘ Mirusviricota’ genes, including hallmark transcription machinery genes missing in herpesviruses, are closely related homologs of large and giant eukaryotic DNA viruses from another viral realm. The remarkable chimeric attributes of ‘ Mirusviricota ’ provide missing links in the evolution of both herpesviruses and giant viruses. Furthermore, mirusviruses are widespread and transcriptionally active from pole to pole, encoding complex functional traits used during the infection of microbial eukaryotes. The ‘ Mirusviricota ’ prevalence, functional activity, diversification, and atypical evolutionary traits point to a lasting role of mirusviruses in the ecology of marine ecosystems that might have not only predated but also contributed to the emergence of herpesviruses and giant viruses.

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