The Origin of Viruses

Patrick Forterre, Morgan Gaïa

Archeal Virology Unit, Institut Pasteur, Paris, France French National Center for Scientific Research, Institute of Integrative Biology of the Cell, University of Paris-Saclay, Gif sur Yvette, France.

Abstract

If viruses are defined by their specific mode of reproduction, i.e., the production of virions, they should have originated after the emergence of the ribosome, since the simplest virion contains at least one protein. Viruses most likely evolved from RNA replicons that recruited genes encoding RNA-binding proteins suitable for capsid or nucleocapsid formation. The first mechanisms for virion egress, dissemination, and cell fusion were possibly related to extracellular vesicles formations. The first viruses were probably RNA viruses, followed by reverse-transcribing RNA viruses – maybe involved in the RNA to DNA transition – and finally DNA viruses. Modern RNA viruses sharing homologous reverse-transcriptases have been grouped in the Riboviria realm and might be the descendants of the first RNA viruses. However, one cannot exclude that the ancient cellular RNA world was populated by other RNA viruses’ lineages now extinct and that Riboviria originated later. Similarly, it is unclear if cosmopolitan DNA viruses of the Varidnaviria and Duplodnaviria realms that have members infecting the three domains of life, Archaea, Bacteria, and Eukarya, are the descendants of ancient viruses that already thrived at the time of the last universal common ancestor (LUCA) or if they originated during the divergence of the three cellular domains. The origin of viruses infecting eukaryotes remains especially enigmatic since they correspond to most known RNA viruses that are rare in Bacteria and unknown in Archaea. Moreover, DNA viruses infecting eukaryotes are more closely related to those infecting Bacteria than to those infecting Archaea, in contradiction with the position of eukaryotes in the tree of life. Hopefully, the future discovery of more viral lineages and a better understanding of the tree of life topology will help to solve this conundrum.

Key words: DNA origin, DNA viruses, LUCA, Reverse transcriptase, RNA viruses, RNA world, Selfish replicons, Virions, Virocells.