A phylogenomic data-driven exploration of viral origins and evolution

Nasir, Arshan; Caetano-Anollés, Gustavo

Analysis revealed that, despite exhibiting high levels of diversity, viral proteomes retain traces of ancient evolutionary history that can be recovered using advanced bioinformatics approaches. The most parsimonious hypothesis inferred from proteomic data suggests that viruses originated from multiple ancient cells that harbored segmented RNA genomes and coexisted with the ancestors of modern cells. We refer to the viral ancestors as "proto-virocells" to emphasize the cellular nature of ancient viruses and to distinguish them from modern virocells that produce elaborate virions [a virocell is any ribocell that, upon viral infection, produces viral progeny instead of dividing by binary fission; sensu (21, 22) ]. This implies the existence of ancient cellular lineages common to both cells and viruses before the appearance of the "last universal cellular ancestor" that gave rise to modern cells. According to our data, the prolonged pressure of genome and particle size reduction eventually reduced virocells into modern viruses (identified by the complete loss of cellular makeup), whereas other coexisting cellular lineages diversified into modern cells. The cellular nature of viruses is restored when modern viruses (re)take control of the cellular machinery of modern cells or when they integrate into cellular genomes. The model for the origin and evolution of the "viral supergroup" (a collection of seven viral subgroups defined by replicon type and replication strategy), as described in the Baltimore classification (23) , captures the many aspects of viral diversity (for example, host preferences, viral morphologies, and proteomic makeup) and, as we show, is backed by strong support from molecular data.