Origins and Evolution of the Global RNA Virome

Abstract

Viruses with RNA genomes dominate the eukaryotic virome, reaching enormous diversity in animals and plants. The recent advances of metaviromics prompted us to perform a detailed phylogenomic reconstruction of the evolution of the dramatically expanded global RNA virome. The only universal gene among RNA viruses is the RNA-dependent RNA polymerase (RdRp). We developed an iterative computational procedure that alternates the RdRp phylogenetic tree construction with refinement of the underlying multiple sequence alignments. The resulting tree encompasses 4,617 RNA virus RdRps and consists of 5 major branches, 2 of which include positive-sense RNA viruses, 1 is a mix of positive-sense (+) RNA and double-stranded (ds) RNA viruses, and 2 consist of dsRNA and negative-sense (−) RNA viruses, respectively. This tree topology implies that dsRNA viruses evolved from +RNA viruses on at least two independent occasions, whereas -RNA viruses evolved from dsRNA viruses. Reconstruction of RNA virus evolution using the RdRp tree as the scaffold suggests that the last common ancestors of the major branches of +RNA viruses encoded only the RdRp and a single jelly-roll capsid protein. Subsequent evolution involved independent capture of additional genes, particularly, those encoding distinct RNA helicases, enabling replication of larger RNA genomes and facilitating virus genome expression and virus-host interactions. Phylogenomic analysis reveals extensive gene module exchange among diverse viruses and horizontal virus transfer between distantly related hosts. Although the network of evolutionary relationships within the RNA virome is bound to further expand, the present results call for a thorough reevaluation of the RNA virus taxonomy.IMPORTANCEThe majority of the diverse viruses infecting eukaryotes have RNA genomes, including numerous human, animal, and plant pathogens. Recent advances of metagenomics have led to the discovery of many new groups of RNA viruses in a wide range of hosts. These findings enable a far more complete reconstruction of the evolution of RNA viruses than what was attainable previously. This reconstruction reveals the relationships between different Baltimore Classes of viruses and indicates extensive transfer of viruses between distantly related hosts, such as plants and animals. These results call for a major revision of the existing taxonomy of RNA viruses.

OUP accepted manuscript

“…1B). As expected, the free-floating genus Ourmiavirus, which includes plant-associated viruses with tripartite genomes, grouped unambiguously with the narnaviruses (Rastgou et al 2009;Turina et al 2017;Wolf et al 2018), whereas mitoviruses formed a sister clade ( Fig. 1B).…”

“…The narnaviral RdRp is highly divergent from those of other eukaryotic RNA viruses, and shows closer homology to the RdRps of RNA bacteriophages in the family Leviviridae (Rodriguez-Cousiño, Esteban, and Esteban 1991;Esteban, Rodriguez-Cousiño, and Esteban 1992;Wolf et al 2018). Detailed comparative genomic and phylogenetic analyses suggest that the Narnaviridae are descended from a levivirus-like bacteriophage which may have been carried within the bacterial progenitor of mitochondria at the point of eukaryogenesis, followed by loss of the capsid protein giving rise to capsidless ('naked') RNA elements (Koonin, Dolja, and Krupovic 2015;Wolf et al 2018). The escape of a group of these viruses into the cytosol may have given rise to the Narnavirus genus (Koonin and Dolja 2014;Wolf et al 2018).…”

“…Detailed comparative genomic and phylogenetic analyses suggest that the Narnaviridae are descended from a levivirus-like bacteriophage which may have been carried within the bacterial progenitor of mitochondria at the point of eukaryogenesis, followed by loss of the capsid protein giving rise to capsidless ('naked') RNA elements (Koonin, Dolja, and Krupovic 2015;Wolf et al 2018). The escape of a group of these viruses into the cytosol may have given rise to the Narnavirus genus (Koonin and Dolja 2014;Wolf et al 2018).…”

Unraveling virus relationships by structure-based phylogenetic classification

“…Comparison of viral protein structures constitutes an important consideration when establishing the relatedness of proteins from genetically distinct viruses. When combined with modern sequence-based approaches (Simmonds et al 2017;Wolf et al 2018), structure-based phylogenetic analysis (SBPA) has proven to be an invaluable tool for drawing deep evolutionary links between proteins. Here, starting from a basic outline of known SBPA approaches, we discuss how the method has been applied to reveal unique insights into viral protein function and relatedness.…”

An inability to maintain the ribonucleoprotein genomic structure is responsible for host detection of negative-sense RNA viruses

“…Given the data presented, the emergence of negative-sense RNA viruses would seem counterintuitive. Based on recent evolutionary predictions, the current hypothesis concerning the origins of this phylum derive from the rapid expansion of positive-sense RNA viruses which branched off into double stranded RNA viruses thereby providing an opportunity to utilize the negative-sense strand in isolation (Wolf et al, 2018). However, utilizing an RNA genome with negative polarity poses a number of inherent constraints.…”