Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis

Abstract

BackgroundFemale endoparasitic ichneumonid wasps inject virus-like particles into their caterpillar hosts to suppress immunity. These particles are classified as ichnovirus virions and resemble ascovirus virions, which are also transmitted by parasitic wasps and attack caterpillars. Ascoviruses replicate DNA and produce virions. Polydnavirus DNA consists of wasp DNA replicated by the wasp from its genome, which also directs particle synthesis. Structural similarities between ascovirus and ichnovirus particles and the biology of their transmission suggest that ichnoviruses evolved from ascoviruses, although molecular evidence for this hypothesis is lacking.ResultsHere we show that a family of unique pox-D5 NTPase proteins in the Glypta fumiferanae ichnovirus are related to three Diadromus pulchellus ascovirus proteins encoded by ORFs 90, 91 and 93. A new alignment technique also shows that two proteins from a related ichnovirus are orthologs of other ascovirus virion proteins.ConclusionOur results provide molecular evidence supporting the origin of ichnoviruses from ascoviruses by lateral transfer of ascoviral genes into ichneumonid wasp genomes, perhaps the first example of symbiogenesis between large DNA viruses and eukaryotic organisms. We also discuss the limits of this evidence through complementary studies, which revealed that passive lateral transfer of viral genes among polydnaviral, bacterial, and wasp genomes may have occurred repeatedly through an intimate coupling of both recombination and replication of viral genomes during evolution. The impact of passive lateral transfers on evolutionary relationships between polydnaviruses and viruses with large double-stranded genomes is considered in the context of the theory of symbiogenesis.

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

“…In particular, we did not find similarity with ascovirus sequences or structures, a finding that does not support the hypothesis that IVs have an ascovirus origin, as previously suggested [23]. However, the absence of conserved proteins among IV structural protein genes is not completely surprising since several sequencing programs focusing on viral genomes have led to similar findings.…”

Genomic and Proteomic Analyses Indicate that Banchine and Campoplegine Polydnaviruses Have Similar, if Not Identical, Viral Ancestors

“…On the basis of a striking similarity discovered between a family of protein-coding genes found in the encapsidated genome of GfIV, the NTPase-like family (14), and an ascoviral gene, it has been suggested that IVs are derived from an ascoviral ancestor (43). However, the data presented here as well as results presented earlier for campoplegine IVs (17) tend to rule out this scenario, given that none of the IV virion structural proteins bear an ascoviral signature.…”

Amoeba/Amoebal Symbiont Genetic Transfers: Lessons from Giant Virus Neighbours

“…( 10) Ascoviridae evolved from Iridoviridae [97] . ( 11) Ascoviridae integrated into their host's genome and evolved to Polydnaviridae [98] . ( 12 ) Probable gene transfer between a poxvirus and an Iridovirus infecting the same host (see fig.…”

“…Iridoviridae are supposed to have evolved from Phycodnaviridae whereas Ascoviridae have likely evolved from Iridoviridae [97] . It is thought that other obligate endosymbiont viruses of parasitoid wasps, ichnoviruses (family: Polydnaviridae ), emerged from Ascoviridae by lateral transfer of ascoviral genes into wasp genomes [98] . Transfers from the wasp genome to the virus symbiont are also likely to occur since it has recently been demonstrated by Desjardins et al [99] that genes encoding sugar transporters in Glyptapanteles indiensis and Glyptapanteles flavicoxis bracoviral (family: Polydnaviridae ) genomes likely originated from the wasp host.…”