The RNA virome of early metazoans sheds light on long-term virus-host relationships

Abstract

Ctenophores and placozoans arose early in metazoan evolution and are characterized by traits associated with key aspects of animal evolution. Despite the evolutionary significance of ctenophores and placozoans, their RNA viromes are poorly understood. To determine the diversity and evolution of RNA virome in these organisms, particularly whether the viruses present with these ancient host lineages similarly occupy basal phylogenetic positions, we analysed publicly available transcriptome data from the Sequence Read Archive (SRA). Accordingly, we identified 26 putative novel viruses classified into 11 virus groups, including members of the families Flaviviridae and Chuviridae. The novel viruses clustered with those previously identified in vertebrates, invertebrates, plants and fungi. Notably, some virus sequences within the Flaviviridae, Chuviridae, Lispiviridae and Marnaviridae were highly divergent, branching deeply relative to their closest known relatives or forming distinct lineages, in some cases suggesting a divergence early in metazoan evolution. In contrast, viruses within the Birnaviridae, Endornaviridae, Mymonaviridae, Narnaviridae, Phasmaviridae, Orthomyxoviridae, Orthototiviridae, and some viruses within the Picornavirales, exhibited patterns consistent with more recent diversification and host jumping. In addition, RNA viruses were detected across multiple species and tissues within the Ctenophora (including whole organisms and embryos) and Placozoa, expanding their host range and highlighting a largely uncharacterized diversity. Together, these findings expand the known diversity and host range of several virus groups, and shed light on virus evolution in early metazoans, demonstrating both host jumping within aquatic environments and virus host-associations that may span the entirety of animal evolution.