Diversity and evolution of the ribovirian class Stelpaviricetes

Metatranscriptome mining has dramatically expanded the known diversity of ribovirians at all taxonomic levels. We explored in detail the class Stelpaviricetes in the phylum Pisuviricota that so far included 3 orders and 6 recognized virus families, order Stellavirales with family Astroviridae infecting vertebrates, Patatavirales with families Potyviridae, the largest known family of plant ribovirians, and Potyliviridae, and Hypofuvirales consisting of 3 families of viruses associated with phytopathogenic fungi. Using an order-specific collection of Hidden Markov Model profiles for the RNA-dependent RNA polymerase (RdRP), the hallmark protein of ribovirians, we identified 103 putative families within Stelpaviricetes, most of which share a uniform, astrovirus-like genome architecture, encoding three recognizable protein domains, the RdRP, a chymotrypsin-like protease and a single jelly roll capsid protein. The topology of the phylogenetic tree of the RdRP implies that the common ancestor of Stelpaviricetes had an astrovirus-like genome. The ancestor of the order Patatavirales acquired two additional domains, a papain-like protease and a superfamily 2 helicase, whereas the capsid protein was replaced with an unrelated one forming filamentous capsids. The ancestor of Hypofuvirales also encoded a superfamily 2 helicase and, possibly, a papain-like protease, but lost the capsid protein. Hypofuvirales might have derived from Patatavirales or evolved independently from an astro-like ancestor. For the vast majority of Stelpaviricetes identified in metatranscriptomes, host assignment remains elusive. Nevertheless, analysis of endogenous virus elements combined with information on isolated viruses provides some clues, in particular, suggesting that the common ancestor of Potyviridae and Potyliviridae had a fungal host whereas the common ancestor of Stelpaviricetes might have been a protist virus. IMPORTANCEThe enormous diversity of viruses on earth is only now coming to light through extensive metagenome and metatranscriptome mining. Using vast databases of ribovirus genomes, we performed phylogenomic analysis of the class Stelpaviricetes that includes the family of animal viruses Astroviridae and Potyviridae, the largest known family of plant viruses. We identified more than 100 family-level groups of viruses most of which have small, astrovirus-like genomes, likely, resembling the common ancestor of Stelpaviricetes. In contrast, the putative common ancestor of Potyviridae and its sister family Potyliviridae exhibits higher genome complexity that apparently emerged in viruses of fungi. The most plausible scenario for the origin of Potyviridae involves cross-kingdom horizontal virus transfer between plant-associated fungi and plants.