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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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Amino acid sequence comparison resulting from a BLAST search done with the DpAV4 ORF90 as a query, and the best hit corresponding to the protein encoded by the ORF1 of the ichnovirus segment GfV-C20 (Subject; Genbank Acc. N° YP_001029423).
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Figure 2: Amino acid sequence comparison resulting from a BLAST search done with the DpAV4 ORF90 as a query, and the best hit corresponding to the protein encoded by the ORF1 of the ichnovirus segment GfV-C20 (Subject; Genbank Acc. N° YP_001029423).

Mentions: More specifically, in DpAV4, ORF90 encodes a protein of 925 amino acid residues that is 40% similar from position 140 to 925 to a protein of 972 amino acid residues encoded by the ORF1 contained in the segment C20 in the GfIV genome (Fig. 2). These two proteins can therefore be considered putative orthologs. The 480 C-terminal residues of this DpAV4 protein are also 42% similar to the C-terminal domain of the protein homologs encoded by the ORF1 of the D1 and D4 GfIV segments, 36% similar to the N-terminal and the C-terminal domains of the protein encoded by the ORFs 184R and 128L of the iridovirus CIV and LCDV, and 30% similar with those encoded by ORFs 119, 99 and 78 in the ascovirus genomes of HvAV3e, SfAV1a and TnAV2c, respectively. Overall, this indicates that this DpAV4 protein is more closely related to that of GfIV than to those found in other ascovirus and iridovirus genomes currently available in databases. ORF091 encodes a protein of 161 amino acid residues similar only with the C-terminal domain of three proteins encoded by the ORFs 1, 1 and 3, contained, respectively, in GfIV segments D1, D4 and D3. In contrast, ORF93 is closer to iridovirus and ascovirus genes than to GfIV genes. This protein of 849 amino acid residues is 43% similar over all its length to CIV ORF184R orthologs in all iridoviral and ascoviral genomes and is only 36% similar over 350 amino acid residues to the C-terminal domain of the GfIV protein homologs encoded by the ORF1, 2, 1, 1, 1 and 1 in, respectively, the C20, C21, D1, D2, D3 and D4 segments of this virus.


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

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

Amino acid sequence comparison resulting from a BLAST search done with the DpAV4 ORF90 as a query, and the best hit corresponding to the protein encoded by the ORF1 of the ichnovirus segment GfV-C20 (Subject; Genbank Acc. N° YP_001029423).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Amino acid sequence comparison resulting from a BLAST search done with the DpAV4 ORF90 as a query, and the best hit corresponding to the protein encoded by the ORF1 of the ichnovirus segment GfV-C20 (Subject; Genbank Acc. N° YP_001029423).
Mentions: More specifically, in DpAV4, ORF90 encodes a protein of 925 amino acid residues that is 40% similar from position 140 to 925 to a protein of 972 amino acid residues encoded by the ORF1 contained in the segment C20 in the GfIV genome (Fig. 2). These two proteins can therefore be considered putative orthologs. The 480 C-terminal residues of this DpAV4 protein are also 42% similar to the C-terminal domain of the protein homologs encoded by the ORF1 of the D1 and D4 GfIV segments, 36% similar to the N-terminal and the C-terminal domains of the protein encoded by the ORFs 184R and 128L of the iridovirus CIV and LCDV, and 30% similar with those encoded by ORFs 119, 99 and 78 in the ascovirus genomes of HvAV3e, SfAV1a and TnAV2c, respectively. Overall, this indicates that this DpAV4 protein is more closely related to that of GfIV than to those found in other ascovirus and iridovirus genomes currently available in databases. ORF091 encodes a protein of 161 amino acid residues similar only with the C-terminal domain of three proteins encoded by the ORFs 1, 1 and 3, contained, respectively, in GfIV segments D1, D4 and D3. In contrast, ORF93 is closer to iridovirus and ascovirus genes than to GfIV genes. This protein of 849 amino acid residues is 43% similar over all its length to CIV ORF184R orthologs in all iridoviral and ascoviral genomes and is only 36% similar over 350 amino acid residues to the C-terminal domain of the GfIV protein homologs encoded by the ORF1, 2, 1, 1, 1 and 1 in, respectively, the C20, C21, D1, D2, D3 and D4 segments of this virus.

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