Viruses are not always harmful: they can provide new functions to the animals they usually infect. The most striking example is probably the utilization by parasitic wasps named Cotesia of a virus that became integrated into their genome 100 million years ago. These wasps attack caterpillars into which their larvae develop. To do this, they produce virus particles, called bracoviruses, that are massively injected, along with their eggs, into the body of caterpillars. The particles infect host cells and the viral genes thus introduced ensure production of proteins necessary for parasitism success. These factors alter immune defenses allowing wasp larvae to survive and develop inside the caterpillar.

An international consortium (France, Netherlands, Brazil, United States) has recently shown (Communications Biology 01/22/2021, doi:10.1038/s42003-020-01623-8) that these virus genes have colonized all chromosomes of the wasps. Contrary to other viruses integrated into genomes that usually decay and are eventually lost, this endogenous bracovirus has undergone such a large genomic expansion that it became a “giant virus”. The virus sequences are dispersed all over the wasp genome, however some conserved regions contain clusters of genes involved in essential viral functions, including particle production and replication of packaged DNA genome. The largest of these regions makes up most of the short arm of one chromosome. Despite a massive production of particles, immune response is not induced, suggesting the wasp no longer perceives the bracovirus as a foreign. It seems that no conflict remains between partners and that the virus functions have been completely integrated in wasp physiology. Virus high-jacking has occurred repeatedly during parasitic wasp evolution suggesting domestication of complex viruses allowing the gene delivery to targeted organisms is a general process of evolution.

Carte de l’organisation des gènes du bracovirus dans le génome de la guêpe parasite Cotesia A. Les différentes localisations des gènes du bracovirus sur les chromosomes de Cotesia congregata sont représentées par des disques colorés dont la taille est proportionnelle au nombre de gènes. En bleu: régions du génome contenant les gènes de virulence incorporés dans les particules et exprimés dans les chenilles parasitées. Noter l’importance de la région située sur le bras court du Chromosome 5. En rouge: régions contenant les gènes impliqués dans la production des particules virales. La région virale du chromosome 7 en contient presque la moitié, si l’on ne compte pas les copies supplémentaires de gènes dispersées produites par duplications. Elle est amplifiée lors de la production des particules et code en particulier pour des composants structuraux majeurs des particules. Les disques en rouge plus foncé correspondent à une famille de gènes hyper-diversifiée par duplications comprenant 35 copies dont jusqu’à 10 sont localisées au même site (C8). B Macro-photographie de la guêpe C. congregata (crédit Hans Smid). — Map of the organization of the genes of the bracovirus in the genome of the parasitic wasp Cotesia A. The different locations of the genes of the bracovirus on the chromosomes of Cotesia congregata are represented by colored discs whose size is proportional to the number of genes. In blue: regions of the genome containing the virulence genes incorporated in the particles and expressed in parasitized caterpillars. Note the importance of the region located on the short arm of Chromosome 5. In red: regions containing the genes involved in the production of viral particles. The viral region of chromosome 7 contains almost half of it, if one does not count extra copies of scattered genes produced by duplications. It is amplified during the production of the particles and in particular codes for major structural components of the particles. The darker red discs correspond to a family of genes hyper-diversified by duplications comprising 35 copies of which up to 10 are located at the same site (C8). B Macro-photograph of the wasp C. congregata (credit Hans Smid).

cotesia 6 especes — Photos of individuals of the six Cotesia species whose genome has been deciphered (credit H. Smid and R. Copeland)

Publication

Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization. Jérémy Gauthier, Hélène Boulain, Joke J.F.A. van Vugt, Lyam Baudry, Emma Persyn, Jean-Marc Aury, Benjamin Noel, Anthony Bretaudeau, Fabrice Legeai, Sven Warris, Mohamed Amine Chebbi, Géraldine Dubreuil, Bernard Duvic, Natacha Kremer, Philippe Gayral, Karine Musset, Thibaut Josse, Diane Bigot, Christophe Bressac, Sébastien Moreau, Georges Periquet, Myriam Harry, Nicolas Montagné, Isabelle Boulogne, Mahnaz Sabeti-Azad, Martine Maïbèche, Thomas Chertemps, Frédérique Hilliou, David Siaussat, Joelle Amselem, Isabelle Luyten, Claire Capdevielle-Dulac, Karine Labadie, Bruna Laïs Merlin, Valérie Barbe, Jetske G. de Boer, Martial Marbouty, Fernando Luis Cônsoli, Stéphane Dupas, Aurélie Hua Van, Gaelle Le Goff, Annie Bézier, Emmanuelle Jacquin-Joly, James B. Whitfield, Louise E.M. Vet, Hans M. Smid, Laure Kaiser-Arnault, Romain Koszul, Elisabeth Huguet, Elisabeth A. Herniou and Jean-Michel Drezen. Communications Biology.Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization. Jérémy Gauthier, Hélène Boulain, Joke J.F.A. van Vugt, Lyam Baudry, Emma Persyn, Jean-Marc Aury, Benjamin Noel, Anthony Bretaudeau, Fabrice Legeai, Sven Warris, Mohamed Amine Chebbi, Géraldine Dubreuil, Bernard Duvic, Natacha Kremer, Philippe Gayral, Karine Musset, Thibaut Josse, Diane Bigot, Christophe Bressac, Sébastien Moreau, Georges Periquet, Myriam Harry, Nicolas Montagné, Isabelle Boulogne, Mahnaz Sabeti-Azad, Martine Maïbèche, Thomas Chertemps, Frédérique Hilliou, David Siaussat, Joelle Amselem, Isabelle Luyten, Claire Capdevielle-Dulac, Karine Labadie, Bruna Laïs Merlin, Valérie Barbe, Jetske G. de Boer, Martial Marbouty, Fernando Luis Cônsoli, Stéphane Dupas, Aurélie Hua Van, Gaelle Le Goff, Annie Bézier, Emmanuelle Jacquin-Joly, James B. Whitfield, Louise E.M. Vet, Hans M. Smid, Laure Kaiser-Arnault, Romain Koszul, Elisabeth Huguet, Elisabeth A. Herniou and Jean-Michel Drezen. Communications Biology.