Recurrent DNA virus domestication leading to different parasite virulence strategies

Abstract

Relics of ancient infections are abundant in eukaryote genomes, but little is known about how they evolve when they confer a functional benefit on their host. We show here, for the first time, that the virus-like particles shown to protect Venturia canescens eggs against host immunity are derived from a nudivirus genome incorporated by the parasitic wasp into its own genetic material. Nudivirus hijacking was also at the origin of protective particles from braconid wasps. However, we show here that the viral genes produce "liposomes" that wrap and deliver V. canescens virulence proteins, whereas the particles are used as gene transfer agents in braconid wasps. Our findings indicate that virus domestication has occurred repeatedly during parasitic wasp evolution but with different evolutionary trajectories after endogenization, resulting in different virulence molecule delivery strategies.

Keywords: Microbiology; genomes; virus domestication; wasps.

Fig. 1. VLP morphogenesis in V. canescens calyx cells.

(A to E) Transmission electron micrographs of (A) calyx cells displaying hypertrophic nuclei (N) containing virogenic stroma (VS) and VLPs; (B) calyx cell nuclei with empty envelopes close to the VS; (C) envelopes filled with VS material giving rise to VLPs; (D) VLPs budding from the calyx cell membrane; (E) immunogold labeling of VS and VLPs in the nucleus with specific antibodies against VLP2 (left) and PIF-0 (right). (Insets) Larger magnifications of VLPs. CYT, cytoplasm; Mv, microvilli of the cytoplasmic membrane; OvL, oviduct lumen; Pm, plasma membrane.

Fig. 2. Organization, origin, and putative function of the nudiviral genes of the V. canescens genome.

(A) Nudiviral genes (in red; named after their OrNV homologs) are grouped into six clusters flanked by regions containing conserved wasp genes (in blue). (B) Phylogenetic tree of insect large double-stranded DNA viruses obtained by maximum likelihood analysis with a concatenated multiple alignment for 37 genes showing that the nudiviruses captured by the V. canescens and braconid wasp lineages belonged to different clades. VcVLP, V. canescens VLP. (C) Genes common to nudiviruses and baculoviruses conserved in V. canescens (red) or wasps carrying bracoviruses (BV) (purple). The products of the helicase gene and of the genes mediating viral gene transcription are not incorporated into the particles (hatched motif). Note that V. canescens lacks capsid genes, consistent with the absence of DNA in the particles.

Fig. 3. Overview of the production, function, and origin of V. canescens VLPs.

(A) VLPs consist of virulence proteins of wasp origin wrapped in nudiviral envelopes. VLPs are released into the oviduct lumen, where they become attached to the wasp egg. Once in the parasitized caterpillar host, VLPs confer immune protection to the egg by impairing capsule formation by the host immune cells. (B) Recurrent virus domestication during parasitic wasp evolution. Two virus genome integration events have occurred during the evolution of campoplegine wasps: the first involved a genome, making it possible to produce ichnoviruses (mediating gene transfer), and the second involved an alphanudivirus genome used for VLP production (mediating the delivery of virulence proteins), which has replaced the ichnovirus in V. canescens. A betanudivirus was independently acquired by a braconid wasp ancestor and gave rise to bracoviruses (DNA delivery).