Genomic and Proteomic Analyses Indicate that Banchine and Campoplegine Polydnaviruses Have Similar, if Not Identical, Viral Ancestors

Abstract

Polydnaviruses form a group of unconventional double-stranded DNA (dsDNA) viruses transmitted by endoparasitic wasps during egg laying into caterpillar hosts, where viral gene expression is essential to immature wasp survival. A copy of the viral genome is present in wasp chromosomes, thus ensuring vertical transmission. Polydnaviruses comprise two taxa, Bracovirus and Ichnovirus, shown to have distinct viral ancestors whose genomes were "captured" by ancestral wasps. While evidence indicates that bracoviruses derive from a nudivirus ancestor, the identity of the ichnovirus progenitor remains unknown. In addition, ichnoviruses are found in two ichneumonid wasp subfamilies, Campopleginae and Banchinae, where they constitute morphologically and genomically different virus types. To address the question of whether these two ichnovirus subgroups have distinct ancestors, we used genomic, proteomic, and transcriptomic analyses to characterize particle proteins of the banchine Glypta fumiferanae ichnovirus and the genes encoding them. Several proteins were found to be homologous to those identified earlier for campoplegine ichnoviruses while the corresponding genes were located in clusters of the wasp genome similar to those observed previously in a campoplegine wasp. However, for the first time in a polydnavirus system, these clusters also revealed sequences encoding enzymes presumed to form the replicative machinery of the progenitor virus and observed to be overexpressed in the virogenic tissue. Homology searches pointed to nucleocytoplasmic large DNA viruses as the likely source of these genes. These data, along with an analysis of the chromosomal form of five viral genome segments, provide clear evidence for the relatedness of the banchine and campoplegine ichnovirus ancestors. IMPORTANCERecent work indicates that the two recognized polydnavirus taxa, Bracovirus and Ichnovirus, are derived from distinct viruses whose genomes integrated into the genomes of ancestral wasps. However, the identity of the ichnovirus ancestor is unknown, and questions remain regarding the possibility that the two described ichnovirus subgroups, banchine and campoplegine ichnoviruses, have distinct origins. Our study provides unequivocal evidence that these two ichnovirus types are derived from related viral progenitors. This suggests that morphological and genomic differences observed between the ichnovirus lineages, including features unique to banchine ichnovirus genome segments, result from evolutionary divergence either before or after their endogenization. Strikingly, analysis of selected wasp genomic regions revealed genes presumed to be part of the replicative machinery of the progenitor virus, shedding new light on the likely identity of this virus. Finally, these genes could well play a role in ichnovirus replication as they were overexpressed in the virogenic tissue. W asps that lay their eggs within the body cavity of caterpillars spend their larval life as endoparasites. Feeding on caterpillar tissues culminates in h...

A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps

“…Our results document a novel domestication event of viruses in parasitic wasps. Indeed, from a function point of view, the domestication we document here is very similar to what has been described in the microgastroid complex in Braconidae [4], in Campopleginae [68], and in Banchinae [3]. In all cases, it is thought that a single endogenization event led to the integration of viral DNA into wasp chromosomes, and subsequently to the evolution of a virallyderived system delivering virulence factors to host immune cells.…”

“…Regarding this question, very few data are available up to now. In two probably independant cases (PDV in campopleginae such as H. dydimator and in banchinae such as Glypta fumiferanae) the ancestral virus has not been clearly identified [68] [3]. On the contrary, the putative virus donors have been identified as beta-nudivirus for PDVs in braconidae [4], and as an alphanudivirus for VLPs found in Venturia canescens [57].…”

RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps

“…To the best of our knowledge, the data presented in this paper represent the first functional analysis of virus-derived particle production in an ichneumonid wasp. Prior to this study, we knew only that the ichnovirus lineage derives from the capture of an unknown viral genome [18,20]. While the main steps of particle production had been studied in the past using TEM, nothing was known about how the genes involved, comprising the so-called IVSPER genes, functioned.…”

“…The genes involved in BV virion production are thus related to nudiviral genes, knowledge that facilitated the assignment of their functional roles [19]. Conversely, the origin of the other PDV taxon, the ichnoviruses (IVs), while certainly viral [18,20], is presently unknown.…”

“…In the genome of icheumonid wasps producing virus-derived particles, the genes putatively derived from the viral ancestor are located in genomic regions named IVSPERs (for Ichno-Virus Structural Protein Encoding Regions; [18]). All IVSPER genes are expressed specifically in the calyx of female wasps, and a number encode proteins that were detected by mass spectrometry analysis of purified IV particles [18,20]. However, because they have no similarities in databases, the functions of these genes have remained unknown.…”