Redefining the invertebrate RNA virosphere

Abstract

Current knowledge of RNA virus biodiversity is both biased and fragmentary, reflecting a focus on culturable or disease-causing agents. Here we profile the transcriptomes of over 220 invertebrate species sampled across nine animal phyla and report the discovery of 1,445 RNA viruses, including some that are sufficiently divergent to comprise new families. The identified viruses fill major gaps in the RNA virus phylogeny and reveal an evolutionary history that is characterized by both host switching and co-divergence. The invertebrate virome also reveals remarkable genomic flexibility that includes frequent recombination, lateral gene transfer among viruses and hosts, gene gain and loss, and complex genomic rearrangements. Together, these data present a view of the RNA virosphere that is more phylogenetically and genomically diverse than that depicted in current classification schemes and provide a more solid foundation for studies in virus ecology and evolution.

Expansion of the Metazoan Virosphere: Progress, Pitfalls, and Prospects

“…And, for both DNA and RNA viruses, contaminating sequences are likely to be at relatively low titre while the copy-number of inherited EVEs will match the host genome. This means that high copy-number itself provides an argument in favour of viral status (Shi et al 2016a).…”

“…First, the nature and quantity of the nucleic acid provides useful clues. Endogenous DNA copies can be identified by a comparison of PCR and RT-PCR (or DNA and RNA sequencing) (Webster et al 2015;Shi et al 2016a;Medd et al 2018;Waldron et al 2018). Functional DNA viruses must express their proteins, so the absence of viral mRNAs argues against active replication.…”

“…It has also discovered new deep branches, such as clades of insectinfecting Partitiviruses (Webster et al 2015;Shi et al 2016a) and Luteo/Sobemo-like viruses (Tokarz et al 2014;Shi et al 2016a), and whole new families, such as the Chuviruses (Li et al 2015). This in turn has led to renewed interest in inferring deep viral phylogenies (Koonin et al 2015;Shi et al 2016a), and has prompted proposals for large-scale updates of higher-level virus taxonomy (Aiewsakun and Simmonds 2018). More importantly, metagenomics now contributes to our thinking on virus evolution.…”

“…More importantly, metagenomics now contributes to our thinking on virus evolution. It has provided a better perspective on host-association and switching (Geoghegan et al 2017;Dolja and Koonin 2018;Shi et al 2018), found familiar virus lineages with unexpected genome sizes and structures (Li et al 2015;Shi et al 2016a;Shi et al 2016b), and uncovered an unexpectedly dynamic history of 'modular' protein swapping (Koonin et al 2015;Shi et al 2016a). Finally, merely having a PCR product from a metagenomic sample can provide an experimental route to the functional biology of an uncultured virus (van Mierlo et al 2014).…”

“…Tokarz et al 2018). The focus has subsequently expanded to include neglected animal lineages, identifying hundreds of new RNA viruses in arthropods and other invertebrates (Webster et al 2015;Shi et al 2016a;Roberts et al 2018;Waldron et al 2018), and recently in divergent and under-sampled chordates (Geoghegan et al 2018;Shi et al 2018).…”