Les virus à nouveau sur le devant de la scène

The great virus comeback

¹ Université Paris-Sud, Institut de Génétique Microbiologie, CNRS UMR 8621, 91405 Orsay Cedex, France
² Institut Pasteur, 25 rue du Dr Roux, 75015 Paris, France

Auteur correspondant : Patrick Forterre, forterre@pasteur.fr

Reçu : 2 Mai 2013

Résumé

Les virus ont longtemps été considérés comme des sous-produits de l’évolution biologique. Cette vision est en train de changer à la suite d’une série de découvertes récentes, la plus frappante étant celle des virus géants. Les virus apparaissent maintenant beaucoup plus vieux, complexes, et divers que l’on a pu l’imaginer. Les virus peuvent être définis comme des organismes qui se multiplient en produisant des virions. Cette définition exclut les ARN infectieux (parfois officiellement classés avec les virus) et implique l’existence d’au moins une protéine virale pour pouvoir parler de virion. Les virus sont donc probablement apparus après les cellules à ARN et protéines, mais avant LUCA, le dernier ancêtre commun à toutes les cellules modernes. Par ailleurs, l’assimilation classique du virus au virion a été remise en cause. L’infection entraîne la formation d’une « cellule virale » (virocell) qui possède tous les attributs d’un être vivant. Le concept de virocell met l’accent sur la phase intracellulaire du cycle viral, pendant laquelle s’exprime la « créativité » du virus, pouvant conduire à l’apparition de nouvelles protéines virales. Les virus sont la source principale de variation et de sélection, les deux piliers du schéma d’évolution darwinienne. Ces données placent les virus au centre du processus évolutif (moteur de l’évolution) et conduisent à les considérer comme des organismes à part entière.

Abstract

Viruses have been considered for a long time as by-products of biological evolution. This view is changing now as a result of several recent discoveries. Viral ecologists have shown that viral particles are the most abundant biological entities on our planet, whereas metagenomic analyses have revealed an unexpected abundance and diversity of viral genes in the biosphere. Comparative genomics have highlighted the uniqueness of viral sequences, in contradiction with the traditional view of viruses as pickpockets of cellular genes. On the contrary, cellular genomes, especially eukaryotic ones, turned out to be full of genes derived from viruses or related elements (plasmids, transposons, retroelements and so on). The discovery of unusual viruses infecting archaea has shown that the viral world is much more diverse than previously thought, ruining the traditional dichotomy between bacteriophages and viruses. Finally, the discovery of giant viruses has blurred the traditional image of viruses as small entities. Furthermore, essential clues on virus history have been obtained in the last ten years. In particular, structural analyses of capsid proteins have uncovered deeply rooted homologies between viruses infecting different cellular domains, suggesting that viruses originated before the last universal common ancestor (LUCA). These studies have shown that several lineages of viruses originated independently, i.e., viruses are polyphyletic. From the time of LUCA, viruses have coevolved with their hosts, and viral lineages can be viewed as lianas wrapping around the trunk, branches and leaves of the tree of life. Although viruses are very diverse, with genomes encoding from one to more than one thousand proteins, they can all be simply defined as organisms producing virions. Virions themselves can be defined as infectious particles made of at least one protein associated with the viral nucleic acid, endowed with the capability to protect the viral genome and ensure its delivery to the infected cell. These definitions, which clearly distinguish viruses from plasmids, suggest that infectious RNA molecules that only encode an RNA replicase presently classified among viruses by the ICTV (International Committee for the Taxonomy of Viruses) into families of Endornaviridae and Hypoviridae are in fact RNA plasmids. Since a viral genome should encode for at least one structural protein, these definitions also imply that viruses originated after the emergence of the ribosome in an RNA-protein cellular world. Although virions are the hallmarks of viruses, viruses and virions should not be confused. The infection transforms the ribocell (cell encoding ribosomes and dividing by binary fission) into a virocell (cell producing virions) or ribovirocell (cell that produces virions but can still divide by binary fission). In the ribovirocell, two different organisms, defined by their distinct evolutionary histories, coexist in symbiosis in the same cell. The virocells or ribovirocells are the living forms of the virus, which can be in fine considered to be a living organism. In the virocell, the metabolism is reorganized for the production of virions, while the ability to capture and store free energy is retained, as in other cellular organisms. In the virocell, viral genomes replicate, recombine and evolve, leading to the emergence of new viral proteins and potentially novel functions. Some of these new functions can be later on transferred to the cell, explaining how viruses can play a major (often underestimated) role in the evolution of cellular organisms. The virocell concept thus helps to understand recent hypotheses suggesting that viruses played a critical role in major evolutionary transitions, such as the origin of DNA genomes or else the origin of the eukaryotic nucleus. Finally, it is more and more recognized that viruses are the major source of variation and selection in living organisms (both viruses and cells), the two pillars of darwinism. One can thus conclude that the continuous interaction between viruses and cells, all along the history of life, has been, and still is, a major engine of biological evolution.