Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Author:

Gauthier Jérémy,Boulain Hélène,van Vugt Joke J. F. A.,Baudry Lyam,Persyn Emma,Aury Jean-MarcORCID,Noel Benjamin,Bretaudeau Anthony,Legeai Fabrice,Warris Sven,Chebbi Mohamed A.,Dubreuil Géraldine,Duvic Bernard,Kremer NatachaORCID,Gayral Philippe,Musset Karine,Josse Thibaut,Bigot Diane,Bressac Christophe,Moreau Sébastien,Periquet Georges,Harry Myriam,Montagné Nicolas,Boulogne Isabelle,Sabeti-Azad Mahnaz,Maïbèche Martine,Chertemps Thomas,Hilliou Frédérique,Siaussat David,Amselem Joëlle,Luyten Isabelle,Capdevielle-Dulac Claire,Labadie Karine,Merlin Bruna Laís,Barbe Valérie,de Boer Jetske G.,Marbouty Martial,Cônsoli Fernando LuisORCID,Dupas Stéphane,Hua-Van AurélieORCID,Le Goff Gaelle,Bézier Annie,Jacquin-Joly EmmanuelleORCID,Whitfield James B.,Vet Louise E. M.,Smid Hans M.,Kaiser Laure,Koszul Romain,Huguet ElisabethORCID,Herniou Elisabeth A.,Drezen Jean-Michel

Abstract

AbstractEndogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

Funder

Agence Nationale de la Recherche

Publisher

Springer Science and Business Media LLC

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,Medicine (miscellaneous)

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