“<i>Paraxenoviridae</i>”, a putative family of globally distributed marine bacteriophages with double-stranded RNA genomes

Abstract Metatranscriptome sequencing dramatically expanded the known diversity of the global RNA virome and, in particular, suggested several new candidate phyla in riboviruses. Using a double-stranded RNA (dsRNA) sequencing, here, we report five complete, bisegmented RNA genomes of a putative phylum group, paraxenoviruses, identified from marine environments. Phylogenetic analysis of the RNA-directed RNA polymerases of paraxenoviruses demonstrated their affinity with the ribovirus order Durnavirales within the class Duplopiviricetes of the phylum Pisuviricota. The order Durnavirales includes families Cystoviridae that consists of well-characterized dsRNA bacteriophages and less thoroughly studied Picobirnaviridae that are also suspected to infect bacteria. Consistently, modeling and analysis of the structure of the predicted capsid protein (CP) of several paraxenoviruses revealed similarity to picobirnavirus CP although the paraxenovirus CP is much larger and contains unique structural elaborations. Taken together, these affinities suggest that paraxenoviruses represent a distinct family within Durnavirales, which we provisionally name “Paraxenoviridae”. Both genomic segments in Picobirnaviridae and “Paraxenoviridae” encompass multiple open reading frames, each preceded by a typical bacterial ribosome-binding site, strongly suggesting that these families consist of bacterial viruses. Search for homologs of paraxenovirus genes shows widespread distribution of this virus group in the global ocean, suggesting an important contribution to marine microbial ecosystems. Our findings further expand the diversity and ecological role of the bacterial RNA virome, reveal extensive structural variability of RNA viral CPs, and demonstrate the common ancestry of several distinct families of bacterial viruses with dsRNA genomes.