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Most double-stranded DNA viruses are classified into two major realms: Duplodnaviria and Varidnaviria. Duplodnaviria comprises tailed bacteriophages and related archaeal viruses of the class Caudoviricetes as well as eukaryotic viruses of the order Herpesvirales. Varidnaviria includes large and giant eukaryotic DNA viruses from the phylum Nucleocytoviricota as well as smaller viruses with tailless icosahedral capsids. The two realms were established on the basis of the non-homologous sets of virion morphogenesis genes (virion module), including those encoding the structurally unrelated major capsid proteins (MCPs) with the ‘double jelly-roll’ and HK97 folds in Varidnaviria and Duplodnaviria, respectively. Both realms are represented across all domains of life, with the respective ancestors thought to date back to the last universal cellular ancestor.
Within Duplodnaviria, bacterial and archaeal members of the Caudoviricetes exhibit a continuous range of genome sizes, from about 10 kilobases (kb) to >700 kb, whereas herpesviruses, restricted to animal hosts, are more uniform with genomes in the range of 100–300 kb. Herpesviruses probably evolved from bacteriophages, but the lack of related viruses outside the animal kingdom raises questions regarding their exact evolutionary trajectory. Members of the Varidnaviria also exhibit a wide range of genome sizes, from about 10 kb to >2 Mb, but there is a discontinuity in the complexity between large and giant viruses of the Nucleocytoviricota phylum and the rest of varidnaviruses with genomes <50 kb. It has been suggested that Nucleocytoviricota have evolved from a smaller varidnavirus ancestor, but the complexification entailing acquisition of multiple informational genes (informational module) remains to be fully understood.
Viruses within Caudoviricetes and Nucleocytoviricota are prevalent in the sunlit ocean where they play a critical role in regulating the community composition and blooming activity of plankton. Here we carried out a genome-resolved metagenomic survey of planktonic DNA viruses guided by the phylogeny of a single hallmark gene. The survey covers nearly 300 billion metagenomic reads from surface-ocean samples of the Tara Oceans expeditions. We characterized and manually curated hundreds of population genomes that expand the known diversity of Nucleocytoviricota. However, most notably, our survey led to the discovery of plankton-infecting relatives of herpesviruses that form a putative new phylum we dubbed Mirusviricota. The mirusviruses share complex functional traits and are widespread in the sunlit oceans where they actively infect eukaryotes, filling a critical gap in our ecological understanding of plankton. Despite a clear evolutionary relationship to herpesviruses, mirusviruses encode even more genes that have closely related homologues in Nucleocytoviricota. These remarkable chimaeric attributes of Mirusviricota connect two distantly related virus realms, providing key insights into the evolution of eukaryotic DNA viruses.
