Genome-Wide Patterns of Bracovirus Chromosomal Integration into Multiple Host Tissues during Parasitism

Abstract

Bracoviruses are domesticated viruses found in parasitic wasp genomes. They are composed of genes of nudiviral origin involved in particle production and proviral segments encoding virulence genes necessary for parasitism success. During particle production, proviral segments are amplified and individually packaged as DNA circles in nucleocapsids. These particles are injected by parasitic waspstogether with their eggs into host larvae. Bracovirus circles of two wasp species were reported toundergo chromosomal integration in parasitized host hemocytes, through a conserved sequence named Host Integration Motif (HIM). Here, we used bulk Illumina sequencing to survey integrations of Cotesia typhae bracovirus circles in the DNA of its host, the maize corn borer ( Sesamia nonagrioides ) seven days after parasitism. First, assembly and annotation of a high-quality genome for C. typhae enabled us to characterize 27 proviral segments clustered in proviral loci. Using these data, we characterized large numbers of chromosomal integrations (from 12 to 85 events per host haploid genome) for all 16 bracovirus circles containing a HIM. Integrations were found in four S. nonagrioides tissues and in the body of a caterpillar in which parasitism had failed. The 12 remaining circles do not integrate but are maintained at high levels in host tissues. Surprisingly, we found that HIM-mediated chromosomal integration has occurred at least six times accidentally in thewasp germline during evolution. Overall, our study furthers our understanding of wasp-host genome interactions and supports HIM-mediated chromosomal integration as a possible mechanism ofhorizontal transfer from wasps to their hosts. Importance Bracoviruses are endogenous domesticated viruses of parasitoid wasps that are injected together with wasp eggs into wasp host larvae during parasitism. Several studies have shown that some DNA circles packaged into bracovirus particles become integrated into host somatic genomes during parasitism, but the phenomenon has never been studied using non-targeted approaches. Here we use bulk Illumina sequencing to systematically characterize and quantify bracovirus circle integrations that occur in four tissues of the Mediterranean corn borer ( Sesamia nonagrioides ) during parasitism by the Cotesia typhae wasp. Our analysis reveals that all circles containing a host integration motif (HIM) integrate at substantial levels (from 12 to 85 integrations per host cell in total) in all tissues while other circles do not integrate. In addition to shedding new light on wasp-bracovirus-host interaction, our study supports HIM-mediated chromosomal integration of bracovirus as a possible source of wasp-to-host horizontal transfer with long term evolutionary consequences.

Somatic chromosomal integration of polydnavirus during parasitism triggered their germline infiltration in multiple lepidopteran families

“…Comparing normalized IEs per segment revealed a higher number of IEs in the hemolymph than in the fat body and a higher number of IEs at 72h than at 24hpp. These trends hold for all seven integrated segments and are in agreement with earlier findings on BVs (Beck et al 2007;Muller et al 2021).…”

“…CvBV and our earlier study on CtBV (Muller et al 2021) shows that PDV circles undergo massive HIM-mediated chromosomal integration in host tissues during parasitism. We thus sought to assess whether horizontal transfer of PDV circles occurred from wasp to lepidopterans through HIM-mediated chromosomal integration in the germline of lepidopteran hosts, followed by vertical transmission in host populations.…”

“…We only investigated chimeric reads mapping to the HIM because the remaining chimeric reads represent only a very small fraction of all chimeric reads (0.8%). As previously done in our study on Cotesia typhae BV (Muller et al 2021), we studied separately the major part of chimeric reads which map to the J1 and J2 motifs from those mapping outside of these motifs (but still within the HIM). We artificially generated chimeric reads following the method described in Peccoud et al (2018) to compare the number of observed microhomology lengths with the number of expected microhomology lengths if junctions occurred randomly between HdIV HIMs and the S. frugiperda genome.…”

“…Applying the same method to characterize circle integration of an IV and a BV (Muller et al 2021) allows us to directly compare the two systems. Patterns of chromosomal integrations turn out to be highly similar between HdIV and CtBV, in terms of nature -all IEs are mediated by a HIM motif having a similar structure with conserved inverted repeats separated by a short stretch of sequence not conserved -, tissue tropism (hemocytes as preferential target), and numbers of IEs per host cell.…”

“…frugiperda system is questionable. Interestingly, whatever the system (CtBV, DsIV, HdIV), there is an enrichment for microhomologies between the host genome and IV circles at the virus-host junction site, suggesting that host DNA repair mechanisms may be involved in at least a subset of IEs (Muller et al 2021;. In fact, the fraction of junctions involving microhomology is higher for IV than for BV as contrary to BV, for IVs we observe almost no junction involving blunt-ended wasp and host sequences or 1-bp microhomology between them.…”