Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata : insights into the evolutionary dynamics of bracoviruses

Abstract

International audienceBracoviruses represent the most complex endogenous viral elements (EVEs) described to date. Nudiviral genes have been hosted within parasitoid wasp genomes since approximately 100 Ma. They play a crucial role in the wasp life cycle as they produce bracovirus particles, which are injected into parasitized lepidopteran hosts during wasp oviposition. Bracovirus particles encapsidatemultiple dsDNAcircles encoding virulence genes. Their expression in parasitized caterpillars is essential for wasp parasitism success. Here, we report on the genomic organization of the proviral segments (i.e. master sequences used to produce the encapsidated dsDNA circles) present in the Cotesia congregata parasitoid wasp genome. The provirus is composed of a macrolocus, comprising two-thirds of the proviral segments and of seven dispersed loci, each containing one to three segments. Comparative genomic analyses with closely related species gave insights into the evolutionary dynamics of bracovirus genomes. Conserved synteny in the differentwasp genomes showed the orthology of the proviral macrolocus across different species. The nudiviral gene odv-e66-like1 is conserved within themacrolocus, suggesting an ancient co-localization of the nudiviral genome and bracovirus proviral segments. By contrast, the evolution of proviral segments within the macrolocus has involved a series of lineage-specific duplications

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

“…We can focus on two periods in the history of the microgastroid complex [15]. The first period concerns the events around the original viral genome integration over 100 Ma [7], and the second around 17 Ma relates to provirus divergence in Cotesia and Glyptapanteles (figures 1 and 3).…”

“…The integrated form of most nudiviral genes has been identified by analyses of a C. congregata genomic bacterial artificial chromosome clone library (see [15] in this issue). Consistent with nudivirus genome integration in ancestral wasps, half of the nudiviral genes are organized in a cluster within the wasp…”

“…Only one nudiviral gene, the odv-e66-like1 gene, which encodes a particle component in C. inanitus [28], has been found within the conserved proviral macrolocus [15]. This localization of odv-e66-like1 is unlikely to be random and thus sustain the hypothesis that the nudiviral machinery and proviral segments have a common origin [15]. The most important modification in BVs compared with pathogenic viruses resides in the fact that the nudiviral genes, including odv-e66-like1, have lost the ability to be incorporated in viral particles [10].…”

“…No nudiviral genes are contained in this packaged genome. In C. congregata, the proviral segment organization consists of a macrolocus comprising two-third of proviral sequences and seven dispersed loci each with one to three segments (see [15]). Comparisons between Cotesia and Glyptapanteles species [37], which diverged approximately 17 Ma [7], highlighted the homology and the remarkable genomic stability of the proviral integration sites, as orthologous hymenopteran genes were found in the flanking regions (see [15] …”

“…PDV particles are produced only in wasps, but infect cells of the caterpillar host (figure 2). PDV genomes are stably integrated into the genomes of parasitoid wasps [15]. They are composed of (i) proviral segments used to produce the multiple dsDNA circles that encode virulence genes and that are packaged in infectious particles, and of (ii) genes, encoding the so-called viral machinery that produce the particles (figure 2).…”