Are Viruses Taxonomic Units? A Protein Domain and Loop-Centric Phylogenomic Assessment

Abstract

Virus taxonomy uses a Linnaean-like subsumption hierarchy to classify viruses into taxonomic units at species and higher rank levels. Virus species are considered monophyletic groups of mobile genetic elements (MGEs) often delimited by the phylogenetic analysis of aligned genomic or metagenomic sequences. Taxonomic units are assumed to be independent organizational, functional and evolutionary units that follow a ‘natural history’ rationale. Here, I use phylogenomic and other arguments to show that viruses are not self-standing genetically-driven systems acting as evolutionary units. Instead, they are crucial components of holobionts, which are units of biological organization that dynamically integrate the genetics, epigenetic, physiological and functional properties of their co-evolving members. Remarkably, phylogenomic analyses show that viruses share protein domains and loops with cells throughout history via massive processes of reticulate evolution, helping spread evolutionary innovations across a wider taxonomic spectrum. Thus, viruses are not merely MGEs or microbes. Instead, their genomes and proteomes conduct cellularly integrated processes akin to those cataloged by the GO Consortium. This prompts the generation of compositional hierarchies that replace the ‘is-a-kind-of’ by a ‘is-a-part-of’ logic to better describe the mereology of integrated cellular and viral makeup. My analysis demands a new paradigm that integrates virus taxonomy into a modern evolutionarily centered taxonomy of organisms.