Adomaviruses: an emerging virus family provides insights into DNA virus evolution

Diverse eukaryotic dsDNA viruses, including adenoviruses, are thought to have evolved from bacteriophages of the family Tectiviridae. The evolutionary relationship of the small circular dsDNA tumor viruses of the families Papillomaviridae and Polyomaviridae to other DNA virus families remains uncertain. Metagenomic surveys of fish reveal 5 previously unknown circular dsDNA viruses that could become founding members of a distinct viral family. These viruses encode predicted superfamily 3 helicases that are related to the replicative helicases of polyomaviruses and papillomaviruses. Additionally, the new viruses encode a gene cluster coding for homologs of adenovirus-like maturation proteases and putative homologs of adenovirus major and minor capsid proteins. We show that these predicted capsid protein are indeed incorporated into the adomavirus virions. Such combination of genes from unrelated virus families is unprecedented among known DNA viruses. We propose the name “Adomaviridae” for this emerging virus family. Significance Statement Although investigation of the origins of viruses is hampered by the poor conservation of the sequences of many viral genes, substantial progress has been made by applying powerful computational methods to compare key viral proteins. Another challenge for understanding viral evolution is the rampant gene exchange between different groups of viruses, and between viruses and their hosts. We describe a group of fish viruses that possess an unexpected combination of genes. The proteins implicated in virus genome replication have homologs in polyomaviruses and papillomaviruses, whereas the structural gene module is related to the corresponding genes of adenoviruses. The unusual genomic layout of these fish viruses suggests unanticipated evolutionary connections between multiple families of tumor-causing viruses.