A phylogenomic data-driven exploration of viral origins and evolution

Nasir, Arshan; Caetano-Anollés, Gustavo

From the point of view of natural history, our bold conjecture simply invokes the existence of proto-virocells-additional cellular descendants of the last universal ancestor of both modern cells and viruses. The proto-virocells reduced into modern viruses, whereas their siblings diversified into Archaea, Bacteria, and Eukarya. It is important to distinguish proto-virocells from modern-day virocells. Although infection of modern-day virocells may result in virion synthesis and cell lysis (22) , the proto-virocell genomes coexisted in the intracellular environment and reproduced either without lysis (similar to endogenous viruses in cellular genomes or plasmids trapped in cells) or by producing primitive forms of virions. In the absence of the jelly-roll fold and other capsid-associated viral folds (which appeared quite late in our timelines), primitive capsid-like structures could have been built from folds seen in prokaryotic protein nanocompartments or by formation and secretion of membrane vesicles. The prokaryotic protein compartments (such as encapsulins and carboxysomes) are polyhedral protein shells that are morphologically similar to icosahedral viruses [for example, (48) ]. Modern-day viral capsids store nucleic acids, whereas prokaryotic protein compartments store enzymes. Perhaps the switch from storing proteins to storing nucleic acids facilitated viral origins in an ancient cell (48) . In turn, modern cells frequently secrete membrane vesicles to communicate with other cells. These vesicles are also morphologically similar to spherical viruses and can package viral genes and contribute toward viral infection (93) . This vesicle secretion phenomenon is very ancient and could have played roles in the origins of ancient viruses [see (94, 95) for other vesiclerelated scenarios of viral origins]. Both scenarios explain how virions were synthesized in proto-virocells to export viral genetic information. Under this scenario, plasmids and other selfish genetic elements also originated from proto-virocells but did not acquire capsids and remained tightly integrated with the emerging ribocellular makeup.