Egoviruses: distant relatives of poxviruses abundant in the gut microbiomes of humans and animals worldwide

Abstract

AbstractLarge and giant double-stranded DNA viruses within the phylumNucleocytoviricotaare diverse and prevalent in the environment where they substantially affect the ecology and evolution of eukaryotes1–4. Until now, these viruses were only sporadically found in the digestive system of vertebrates5–7. Here, we present the identification and genomic characterization of a proposed third order of viruses within the classPokkesviricetesthat currently consists of poxvirusesand asfuviruses8. Members of this newly identified order we provisionally named “Egovirales” are commonly in the digestive system of vertebrates worldwide and are abundant in >10% of livestock animals, >2% of humans, and wild animals. Egoviruses have linear genomes up to 467 kbp in length and likely form multilayered icosahedral capsids, similar to those of asfuviruses. However, phylogenetic analysis of conserved viral genes indicates that egoviruses are the sister group of poxviruses, with implications for capsid evolution. The diversity of egoviruses already far exceeds that of all known poxviruses and animal-associated asfuviruses. Phylogenetic analyses and patterns of virus distribution across vertebrates suggest that egoviruses can be either specialists or generalists associated with a single or multiple vertebrate species, respectively. Notably, one egovirus clade is human-specific, evolutionarily constrained, and spread across continents, demonstrating a long-term association betweenEgoviralesand the human population on the global scale. Egoviruses not only expand the ecological and evolutionary scope ofPokkesviricetes, but also represent the only diverse, widespread, and abundant group of double-stranded DNA viruses infecting eukaryotic cells in the digestive system of vertebrates.