The origin of viruses remains mysterious because of their diverse and patchy molecular and functional makeup. Although numerous hypotheses have attempted to explain viral origins, none is backed by substantive data. Viruses harboring different replicon types and infecting distantly related hosts shared many metabolic and informational protein structural domains of ancient origin that were also widespread in cellular proteomes. Phylogenomic analysis uncovered a universal tree of life and revealed that modern viruses reduced from multiple ancient cells that harbored segmented RNA genomes and coexisted with the ancestors of modern cells. The model for the origin and evolution of viruses and cells is backed by strong genomic and structural evidence and can be reconciled with existing models of viral evolution if one considers viruses to have originated from ancient cells and not from modern counterparts.
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.
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