Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps

Abstract

Background: Polydnaviruses (PDVs) are mutualistic endogenous viruses inoculated by some lineages of parasitoid wasps into their hosts, where they facilitate successful wasp development. PDVs include the ichnoviruses and bracoviruses that originate from independent viral acquisitions in ichneumonid and braconid wasps respectively. PDV genomes are fully incorporated into the wasp genomes and consist of (1) genes involved in viral particle production, which derive from the viral ancestor and are not encapsidated, and (2) proviral segments harboring virulence genes, which are packaged into the viral particle. To help elucidating the mechanisms that have facilitated viral domestication in ichneumonid wasps, we analyzed the structure of the viral insertions by sequencing the whole genome of two ichnovirus-carrying wasp species, Hyposoter didymator and Campoletis sonorensis. Results: Assemblies with long scaffold sizes allowed us to unravel the organization of the endogenous ichnovirus and revealed considerable dispersion of the viral loci within the wasp genomes. Proviral segments contained species-specific sets of genes and occupied distinct genomic locations in the two ichneumonid wasps. In contrast, viral machinery genes were organized in clusters showing highly conserved gene content and order, with some loci located in collinear wasp genomic regions. This genomic architecture clearly differs from the organization of PDVs in braconid wasps, in which proviral segments are clustered and viral machinery elements are more dispersed. Conclusions: The contrasting structures of the two types of ichnovirus genomic elements are consistent with their different functions: proviral segments are vehicles for virulence proteins expected to adapt according to different host defense systems, whereas the genes involved in virus particle production in the wasp are likely more stable and may reflect ancestral viral architecture. The distinct genomic architectures seen in ichnoviruses versus bracoviruses reveal different evolutionary trajectories that have led to virus domestication in the two wasp lineages.

The Unconventional Viruses of Ichneumonid Parasitoid Wasps

“…Interestingly, G. fumiferanae IVSPERs also contained at least three genes with conserved viral domains, namely a DNA polymerase, a D5 primase-helicase, and a DEXD helicase. Note that homologs for the last two genes were also recently described in H. didymator and C. sonorensis IVSPERs [30]. These domains are found in a set of genes conserved among nucleocytoplasmic large DNA viruses (NCLDVs), an observation that suggests the IV progenitor(s) could be from an uncharacterized or extinct viral taxon related to this group of viruses.…”

“…Furthermore, homologs to HdIV structural genes were identified in the calyx transcriptome of other IV-associated campoplegine wasps, namely Tranosema rostrale [19] and Bathyplectes sp. [24], or in the genome of C. sonorensis [30]. This clearly indicated that the set of virion structural genes was conserved among campoplegine wasps known to produce IVs.…”

“…The recent sequencing of the H. didymator and C. sonorensis genomes [30] led to the identification of two additional IVSPERs and one isolated structural gene in H. didymator, and of four IVSPERs and two singletons in C. sonorensis, adding up to 54 and 48 genes, respectively, in the virus-derived machineries of these two wasp species.…”

“…The recent whole genome sequencing of the two campoplegine wasps, H. didymator and C. sonorensis, revealed an extremely complex ichnovirus genomic architecture [30]. The integrated ichnovirus genome comprises two components that differ in both their features and functions in the virus/parasitoid life cycle: the proviral genome segments and the "replication" genes (Figure 4).…”

“…Globally, IVSPERs are far less numerous than proviral segments [30]. The H. didymator genome contained one isolated IV replication gene and five IVSPERs (with sizes varying from 2 to 27 kb and a number of genes ranging from 2 to 19), adding up to 54 predicted replication genes.…”