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

Fabrice Legeai,Xin Zhou,Bernardo F Santos,Seán G Brady,Anthony Bretaudeau,Bruce A Webb,Jean-Michel Drezen,Marc Ravallec,Stéphanie Robin,Anne-Nathalie Volkoff,Rebecca B Dikow,Denis Tagu,Shanlin Liu,Véronique Jouan,Claire Lemaitre,Gabor Gyapay,Frédéric Baudat

doi:10.1186/s12915-020-00822-3

Abstract

BackgroundPolydnaviruses (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.ResultsAssemblies 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.ConclusionsThe 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.

Highlights

Polydnaviruses (PDVs) are mutualistic endogenous viruses inoculated by some lineages of parasitoid wasps into their hosts, where they facilitate successful wasp development
The C. sonorensis assembled genome consisted of 259 Mb in 11,756 scaffolds with sizes ranging from 400 bp to 6.1 Mbp, with an N50 of 725,399 bp and a contig N50 of 315,222 bp (Table 1)
Our results reveal a clear duality between the proviral segments and the conserved viral machinery, differences that may be linked to the biological functions of these elements

Summary

Introduction

Polydnaviruses (PDVs) are mutualistic endogenous viruses inoculated by some lineages of parasitoid wasps into their hosts, where they facilitate successful wasp development. 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. Parasites and their hosts are involved in a continual coevolutionary arms race, with hosts evolving defense mechanisms and parasites developing strategies to overcome them [1, 2]. PDVs do not replicate but express genes that induce profound physiological alterations in the parasitized host, such as impairment of the immune response or developmental alterations, which are required for successful development of the wasp larva [5,6,7,8,9]

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Conclusion