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Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis.

Bigot Y, Samain S, Augé-Gouillou C, Federici BA - BMC Evol. Biol. (2008)

Bottom Line: Our 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Université François Rabelais de Tours, GICC, UFR des Sciences & Techniques, Parc de Grandmont, 37200 Tours, France. bigot@univ-tours.fr

ABSTRACT

Background: Female 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.

Results: Here 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.

Conclusion: Our 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.

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Map of the 13-kbp region of the DpAV4 genome (EMBL Acc. N°CU469068andCU467486) that contains the gene cluster with direct homologs in the genome of the Glypta fumiferanae ichnovirus. DpAV-4 ORF with well-characterized direct homologs among other ascovirus and iridovirus genomes are represented by white arrows. Homologous ORF of the GfIV genes are represented by black arrows. The sequence and the features of the protein encoded by these ORF are detailed in fig. S1. Below, the graph is scaled in kbp.
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Figure 1: Map of the 13-kbp region of the DpAV4 genome (EMBL Acc. N°CU469068andCU467486) that contains the gene cluster with direct homologs in the genome of the Glypta fumiferanae ichnovirus. DpAV-4 ORF with well-characterized direct homologs among other ascovirus and iridovirus genomes are represented by white arrows. Homologous ORF of the GfIV genes are represented by black arrows. The sequence and the features of the protein encoded by these ORF are detailed in fig. S1. Below, the graph is scaled in kbp.

Mentions: The DpAV4 genome sequenced by Genoscope (France) is 119,334-bp in length. Its organization, gene content and evolutionary characteristics will be detailed in a separate publication (manuscript in preparation; Additional file 1). However, BLAST results obtained with several ORFs in the DpAV4 genome provide evidence that certain ichnovirus ORFs have their closest relatives in an ascovirus genome. Specifically, we identified a 13-kbp region that contains a cluster of three genes (Fig. 1, ORF90, 91 and 93; Additional files 1 and 2) that have close homologs in a GfIV gene family composed of seven members [28]. All contain a domain similar to a conserved domain found in the pox-D5 family of NTPases. To date, this pox-D5 domain has been identified as a NTP binding domain of about 250 amino acid residues found only in viral proteins encoded by poxvirus, iridovirus, ascovirus and mimivirus genomes. These genes seem to be specific to GfIV, as they are absent in the three sequenced genomes of other ichnoviruses, namely CsIV, Tranosema rostrales ichnovirus (TrIV), and Hyposoter fugitivus ichnovirus (HfIV).


Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis.

Bigot Y, Samain S, Augé-Gouillou C, Federici BA - BMC Evol. Biol. (2008)

Map of the 13-kbp region of the DpAV4 genome (EMBL Acc. N°CU469068andCU467486) that contains the gene cluster with direct homologs in the genome of the Glypta fumiferanae ichnovirus. DpAV-4 ORF with well-characterized direct homologs among other ascovirus and iridovirus genomes are represented by white arrows. Homologous ORF of the GfIV genes are represented by black arrows. The sequence and the features of the protein encoded by these ORF are detailed in fig. S1. Below, the graph is scaled in kbp.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2567993&req=5

Figure 1: Map of the 13-kbp region of the DpAV4 genome (EMBL Acc. N°CU469068andCU467486) that contains the gene cluster with direct homologs in the genome of the Glypta fumiferanae ichnovirus. DpAV-4 ORF with well-characterized direct homologs among other ascovirus and iridovirus genomes are represented by white arrows. Homologous ORF of the GfIV genes are represented by black arrows. The sequence and the features of the protein encoded by these ORF are detailed in fig. S1. Below, the graph is scaled in kbp.
Mentions: The DpAV4 genome sequenced by Genoscope (France) is 119,334-bp in length. Its organization, gene content and evolutionary characteristics will be detailed in a separate publication (manuscript in preparation; Additional file 1). However, BLAST results obtained with several ORFs in the DpAV4 genome provide evidence that certain ichnovirus ORFs have their closest relatives in an ascovirus genome. Specifically, we identified a 13-kbp region that contains a cluster of three genes (Fig. 1, ORF90, 91 and 93; Additional files 1 and 2) that have close homologs in a GfIV gene family composed of seven members [28]. All contain a domain similar to a conserved domain found in the pox-D5 family of NTPases. To date, this pox-D5 domain has been identified as a NTP binding domain of about 250 amino acid residues found only in viral proteins encoded by poxvirus, iridovirus, ascovirus and mimivirus genomes. These genes seem to be specific to GfIV, as they are absent in the three sequenced genomes of other ichnoviruses, namely CsIV, Tranosema rostrales ichnovirus (TrIV), and Hyposoter fugitivus ichnovirus (HfIV).

Bottom Line: Our 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Université François Rabelais de Tours, GICC, UFR des Sciences & Techniques, Parc de Grandmont, 37200 Tours, France. bigot@univ-tours.fr

ABSTRACT

Background: Female 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.

Results: Here 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.

Conclusion: Our 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.

Show MeSH
Related in: MedlinePlus