Origin of viruses: primordial replicators recruiting capsids from hosts

Abstract

Viruses are ubiquitous parasites of cellular life and the most abundant biological entities on earth. It is widely accepted that viruses are polyphyletic but a consensus scenario for their ultimate origin(s) is still lacking. Traditionally, three different scenarios have been considered for the origin of viruses: descent from primordial, pre-cellular genetic elements, reductive evolution from cellular ancestors, and escape of genes from cellular hosts achieving partial replicative autonomy and becoming parasitic genetic elements. These three classical scenarios give different timelines for the origin of viruses and do not explain the provenance of the two key functional modules that are responsible, respectively, for virus genome replication and virion morphogenesis. Here we outline a 'chimeric' scenario under which different types of primordial, selfish replicons gave rise to viruses by recruiting host proteins for virion formation. We also propose that new groups of viruses have repeatedly emerged at all stages of the evolution of life, often, through the displacement of ancestral structural and genome replication genes. [H1] Introduction Viruses are the most abundant biological entities on our planet and have major roles in global ecology and evolution of the biosphere 1-4. All cellular organisms, with the possible exception of some intracellular parasitic bacteria, harbour distinctive repertoires of viruses, that is, obligate intracellular genetic parasites that package their genomes into virus particles (virions) 5. The ubiquity of viruses, combined with the theoretical argument that genetic parasites will inevitably emerge in replicator systems 6,7 , implies that the entire course of the evolution of life is actually a story of virus-host coevolution 4,8-10. Accordingly, evolution of life cannot be understood without elucidating the origin(s) of viruses, yet, these origins currently remain mysterious. Historically, three distinct scenarios of virus origin have been considered 11-17 (Figure 1). According to the 'primordial virus world' or 'virus early' hypothesis, viruses are direct descendants of the first replicons that existed during the pre-cellular stage of the evolution of life. By contrast, in the 'reductive virus origin' or 'regression' scenario, viruses are the ultimate products of degeneration of ancestral cells that have lost their autonomy and transitioned to obligate intracellular parasitism. Finally, in the 'escaped genes' scenario, viruses evolved on multiple, independent occasions in different cellular organisms from host genes that acquired the capacity for (quasi)autonomous, selfish replication and infectivity. Accordingly, escaped bacterial, archaeal and eukaryotic genes are thought to have given rise to bacterial, 2 archaeal and eukaryotic viruses, respectively. The three scenarios seem to be mutually exclusive with respect to the origin of any particular group of viruses but different groups of viruses potentially could have evolved via different routes. Over the years, all three scenari...

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