Analysis of Virion Structural Components Reveals Vestiges of the Ancestral Ichnovirus Genome

Anne-Nathalie Volkoff,Véronique Jouan,Gabor Gyapay,Fasseli Coulibaly,Patrick Wincker,Serge Urbach,Fabrice Legeai,Max Bergoin,Bertille Provost,Edith Demettre,Sylvie Samain,Catherine Béliveau,Jean-Michel Drezen,François Cousserans,Michel Cusson

doi:10.1371/journal.ppat.1000923

Abstract

Many thousands of endoparasitic wasp species are known to inject polydnavirus (PDV) particles into their caterpillar host during oviposition, causing immune and developmental dysfunctions that benefit the wasp larva. PDVs associated with braconid and ichneumonid wasps, bracoviruses and ichnoviruses respectively, both deliver multiple circular dsDNA molecules to the caterpillar. These molecules contain virulence genes but lack core genes typically involved in particle production. This is not completely unexpected given that no PDV replication takes place in the caterpillar. Particle production is confined to the wasp ovary where viral DNAs are generated from proviral copies maintained within the wasp genome. We recently showed that the genes involved in bracovirus particle production reside within the wasp genome and are related to nudiviruses. In the present work we characterized genes involved in ichnovirus particle production by analyzing the components of purified Hyposoter didymator Ichnovirus particles by LC-MS/MS and studying their organization in the wasp genome. Their products are conserved among ichnovirus-associated wasps and constitute a specific set of proteins in the virosphere. Strikingly, these genes are clustered in specialized regions of the wasp genome which are amplified along with proviral DNA during virus particle replication, but are not packaged in the particles. Clearly our results show that ichnoviruses and bracoviruses particles originated from different viral entities, thus providing an example of convergent evolution where two groups of wasps have independently domesticated viruses to deliver genes into their hosts.

Highlights

Polydnaviruses (PDVs) are unique viruses symbiotically associated with endoparasitic wasps belonging to the families Braconidae and Ichneumonidae
We recently identified genes encoding structural components of PDVs associated with braconid wasps (Bracoviruses or BVs)
We showed that 11 homologues of H. didymator ichnovirus (HdIV) Ichnovirus Structural Protein Encoding Regions (IVSPERs) genes are expressed in the ovaries of the ichneumonid wasp Tranosema rostrale, indicating that the set of structural genes is conserved among wasps associated with IVs

Summary

Introduction

Polydnaviruses (PDVs) are unique viruses symbiotically associated with endoparasitic wasps belonging to the families Braconidae and Ichneumonidae. Overall the data support the hypothesis that a nudivirus integrated its own genome into that of the ancestor of bracovirus-associated wasps, which lived ,100 million years ago, according to a recent estimation based on the age of fossils in amber [14]. Since their integration into the wasp genome, the original nudivirus genes that were not essential to the parasitoid host interaction appear to have been replaced, in the packaged BV genome, by genes contributing to the success of parasitism. The nudivirus-like genes are expressed in the calyx region of the wasp ovaries, where BV virions are produced, and they have been maintained in Author Summary

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