Genomic and phylogenetic features of thePicobirnaviridaesuggest microbial rather than animal hosts

Abstract

ABSTRACTThe RNA virus familyPicobirnaviridaehas traditionally been associated with the gastrointestinal systems of terrestrial mammals and birds, with the majority of viruses detected in animal stool samples. Metatranscriptomic studies of vertebrates, invertebrates, microbial communities, and environmental samples have resulted in an enormous expansion of the genomic and phylogenetic diversity of this family. Yet picobirnaviruses remain poorly classified, with only one genus and three species formally ratified by the International Committee of Virus Taxonomy. Additionally, an inability to culture picobirnaviruses in a laboratory setting or isolate them in animal tissue samples, combined with the presence of bacterial genetic motifs in their genomes, suggests these viruses may represent RNA bacteriophage rather than being associated with animal infection. Utilising a data set of 2,286 picobirnaviruses sourced from mammals, birds, reptiles, fish, invertebrates, microbial communities, and environmental samples, we identified seven consistent phylogenetic clusters likely representing picobirnavirus genera that we tentatively nameAlpha-, Beta-, Gamma-, Delta-, Epsilon-, Zeta-,andEtapicobirnavirus. A statistical analysis of topological congruence between virus-host phylogenies revealed more frequent cross-species transmission than any other RNA virus family. In addition, bacterial ribosomal binding site motifs were more enriched in picobirnavirus genomes than in the two groups of established RNA bacteriophage – theLeviviricetesandCystoviridae. Overall, our findings support the hypothesis that thePicobirnaviridaehave bacterial hosts and provide a lower-level taxonomic classification for this highly diverse and ubiquitous family of RNA viruses.