In parallel, we are also interested in the diversity of virus-ichneumonid wasp associations

Identification of an ichnoviral machinery in a beetle parasitoid producing atypical particles

In the literature, ichnoviruses are described as being associated with parasitoids of lepidopteran larvae. Species of the genus Bathyplectes, which are campoplegine ichneumonids that parasitize larvae of the alfalfa pest Hypera postica (Coleoptera: Curculionidae), also produce virus particles in their ovaries. However, these particles are atypical compared to classical ichnovirus particles (Figure 4). This raised the question of their nature.

Figure 4. Electron microscopic view of virus particles produced in Bathyplectes sp. (diam. ~200 nm) and Hyposoter sp. (length ~300 nm). Figure taken from the team's publication DOI: 10.1016/j.virusres.2019.02.001.

To find out the nature of these atypical particles, the transcriptome of Bathyplectes anurus ovaries was analyzed (Robin et al, 2019). We were able to identify a total of 28 homologs to genes of the ichnoviral machinery, as well as a few sequences corresponding to genes of the repeat element family, characteristic of the segments encapsidated in the ichnovirus particles of campoplegines. The atypical particles of this parasitoid are therefore related to ichnoviruses.

This work shows the diversity of particles that can be produced by the machinery that derives a priori from a single event of integration of an ancestor viral genome.

Loss of ichnovirus and exaptation of a nudivirus in the lineage of the parasitoid Venturia canescens

Venturia canescens is a campoplegine that parasites stored food pests (e.g. Ephestia kuehniella). This species, although phylogenetically close to ichnovirus-associated species, produces DNA-free particles called virus-like particles (VLPs) (Figure 5). VLPs mainly contain proteins encoded by wasp genes. They associate with the eggs in the lumen of the oviducts and protect the eggs from destruction by the host immune system. Our work has shown that VLPs are derived from the incorporation of an alphanudivirus genome (Pichon et al, 2015). The analysis of the wasp genome also identified deeply reshuffled ichnovirus sequences. This indicates that the ancestor of this wasp was indeed associated with an ichnovirus and that the incorporation of the nudivirus resulted in a viral symbiont replacement. This is the first described example of the replacement of an endogenous virus playing a functional role in the life cycle of the organism that hosts it.

Figure 5. Electron microscopic view of VLPs produced in Venturia canescens. Figure taken from the team's publication DOI: 10.1051/medsci/20163208013.

The V. canescens genome contains 51 functional nudiviral genes, including many nudivirus core genes but no genes encoding capsid proteins or involved in viral DNA packaging, which is consistent with the absence of DNA in VLPs. Further analysis of the V. canescens genome revealed that the genes involved in viral DNA replication and packaging are present as pseudogenes (Leobold et al 2018). This supports the hypothesis that an entire nudivirus genome was initially integrated into a wasp chromosome.

Bracoviruses, the other PDV genus, also derive from the integration of a nudivirus, but different from the one at the origin of VLPs. Thus, our work shows that two independent events of capture of nudivirus genomes in two lineages of parasitoid wasps have led to two modalities of evolution of endogenous viral sequences that result in different strategies of control of host physiology, since bracoviruses allow the transfer of genes whereas VLPs the transfer of proteins towards the parasitoid host.