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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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Sequence (lanes 1 to 3) and secondary structure (lanes 4 to 6) comparisons among (a) MCP and (b) SfAV1a ORF061 orthologs from CsIV (lanes 1 and 4, typed in black), DpAV4 (lanes 2 and 5, typed in blue) and SfAV1a (lanes 3 and 6, typed in purple). Conserved positions among the amino acid sequence of CsIV and those of DpAV4 and SfAV1a are highlighted in grey. Secondary structures in the three SfAV1a ORF061 orthologs were calculated with the Network Protein Sequence Analysis at http://npsa-pbil.ibcp.fr/ and the statistical relevance of the secondary structures were evaluated with Psipred at http://bioinf.cs.ucl.ac.uk/psipred/. C, E and H in lanes 4 to 6 respectively indicated for each amino acid that it is involved in a coiled, b sheet or a helix structure. Using default parameters of Psipred, upper case letters indicate that the predicted secondary structure is statically significant in Psipred results. Significant secondary structures are highlighted in yellow. In (a), the comparisons were limited to three of the seven conserved domains (Additional file 3a, b and 3c), the 2, 5 and 7. Indeed, classical in silico methods appeared to be inappropriate to predict statistically significant secondary structures in conserved structural protein rich in b strand such as iridovirus and ascovirus MCP. In contrast, a complete and coherent domain comparison was obtained by HCA profiles (fig. S3b, c).
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Figure 3: Sequence (lanes 1 to 3) and secondary structure (lanes 4 to 6) comparisons among (a) MCP and (b) SfAV1a ORF061 orthologs from CsIV (lanes 1 and 4, typed in black), DpAV4 (lanes 2 and 5, typed in blue) and SfAV1a (lanes 3 and 6, typed in purple). Conserved positions among the amino acid sequence of CsIV and those of DpAV4 and SfAV1a are highlighted in grey. Secondary structures in the three SfAV1a ORF061 orthologs were calculated with the Network Protein Sequence Analysis at http://npsa-pbil.ibcp.fr/ and the statistical relevance of the secondary structures were evaluated with Psipred at http://bioinf.cs.ucl.ac.uk/psipred/. C, E and H in lanes 4 to 6 respectively indicated for each amino acid that it is involved in a coiled, b sheet or a helix structure. Using default parameters of Psipred, upper case letters indicate that the predicted secondary structure is statically significant in Psipred results. Significant secondary structures are highlighted in yellow. In (a), the comparisons were limited to three of the seven conserved domains (Additional file 3a, b and 3c), the 2, 5 and 7. Indeed, classical in silico methods appeared to be inappropriate to predict statistically significant secondary structures in conserved structural protein rich in b strand such as iridovirus and ascovirus MCP. In contrast, a complete and coherent domain comparison was obtained by HCA profiles (fig. S3b, c).

Mentions: Because ascovirus virions and ichnovirus particles display structural similarities, we developed an approach to search for homologs of virion structural proteins in ichnoviruses. These approaches were initiated in 2000 and recently finalized, but some of the conclusions have been published [14]. To date, only two virion proteins from the Campoletis sonorensis ichnovirus (CsIV) have been characterized [31,32]. The first is the P44 (Acc N° AAD01199), a structural protein that appears to be located as a layer between the out envelope and nucleocapsid, and the second, P12, a capsid protein (Acc N° AF004367). Presently, there are more than one hundred ascoviral or iridoviral MCP sequences in databases. BLAST searches using these sequences failed to detect any similarities between CsIV virion proteins and ascoviral or iridoviral MCPs, or any other proteins [33]. To evaluate the possibility that homology between ichnovirus and ascovirus virion proteins may simply not be detectable by conventional Blastp searches, we used a different method, WAPAM (weighted automata pattern matching; [34]). The models were designed on the basis of a previous study [22] demonstrating that MCP encoded by ascovirus, iridovirus, phycodnavirus and asfarvirus genomes are related, and all contain 7 conserved domains separated by hinges of very variable size. We investigated these conserved domains further using hydrophobic cluster analysis (HCA, [35]). This analysis revealed that most conservation occurred at the level of hydrophobic residues, as expected for structural proteins (Additional file 3a and 3b). The size variability of the hinges between conserved domains and the conservation of hydrophobic residues might explain why BLAST searches using iridoviral and ascoviral MCP sequences have limited ability to detect MCP orthologs in phycodnavirus and asfarvirus genomes. We designed two syntactic models (see Materials and Methods), which together were able to specifically align all MCP sequences of the four virus families. Importantly, WAPAM aligned the CsIV ichnovirus P44 structural protein with both models. Complementary structural and HCA confirmed the presence of the seven conserved domains in this CsIV structural protein (Fig. 3a and Additional file 3c).


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

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

Sequence (lanes 1 to 3) and secondary structure (lanes 4 to 6) comparisons among (a) MCP and (b) SfAV1a ORF061 orthologs from CsIV (lanes 1 and 4, typed in black), DpAV4 (lanes 2 and 5, typed in blue) and SfAV1a (lanes 3 and 6, typed in purple). Conserved positions among the amino acid sequence of CsIV and those of DpAV4 and SfAV1a are highlighted in grey. Secondary structures in the three SfAV1a ORF061 orthologs were calculated with the Network Protein Sequence Analysis at http://npsa-pbil.ibcp.fr/ and the statistical relevance of the secondary structures were evaluated with Psipred at http://bioinf.cs.ucl.ac.uk/psipred/. C, E and H in lanes 4 to 6 respectively indicated for each amino acid that it is involved in a coiled, b sheet or a helix structure. Using default parameters of Psipred, upper case letters indicate that the predicted secondary structure is statically significant in Psipred results. Significant secondary structures are highlighted in yellow. In (a), the comparisons were limited to three of the seven conserved domains (Additional file 3a, b and 3c), the 2, 5 and 7. Indeed, classical in silico methods appeared to be inappropriate to predict statistically significant secondary structures in conserved structural protein rich in b strand such as iridovirus and ascovirus MCP. In contrast, a complete and coherent domain comparison was obtained by HCA profiles (fig. S3b, c).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 3: Sequence (lanes 1 to 3) and secondary structure (lanes 4 to 6) comparisons among (a) MCP and (b) SfAV1a ORF061 orthologs from CsIV (lanes 1 and 4, typed in black), DpAV4 (lanes 2 and 5, typed in blue) and SfAV1a (lanes 3 and 6, typed in purple). Conserved positions among the amino acid sequence of CsIV and those of DpAV4 and SfAV1a are highlighted in grey. Secondary structures in the three SfAV1a ORF061 orthologs were calculated with the Network Protein Sequence Analysis at http://npsa-pbil.ibcp.fr/ and the statistical relevance of the secondary structures were evaluated with Psipred at http://bioinf.cs.ucl.ac.uk/psipred/. C, E and H in lanes 4 to 6 respectively indicated for each amino acid that it is involved in a coiled, b sheet or a helix structure. Using default parameters of Psipred, upper case letters indicate that the predicted secondary structure is statically significant in Psipred results. Significant secondary structures are highlighted in yellow. In (a), the comparisons were limited to three of the seven conserved domains (Additional file 3a, b and 3c), the 2, 5 and 7. Indeed, classical in silico methods appeared to be inappropriate to predict statistically significant secondary structures in conserved structural protein rich in b strand such as iridovirus and ascovirus MCP. In contrast, a complete and coherent domain comparison was obtained by HCA profiles (fig. S3b, c).
Mentions: Because ascovirus virions and ichnovirus particles display structural similarities, we developed an approach to search for homologs of virion structural proteins in ichnoviruses. These approaches were initiated in 2000 and recently finalized, but some of the conclusions have been published [14]. To date, only two virion proteins from the Campoletis sonorensis ichnovirus (CsIV) have been characterized [31,32]. The first is the P44 (Acc N° AAD01199), a structural protein that appears to be located as a layer between the out envelope and nucleocapsid, and the second, P12, a capsid protein (Acc N° AF004367). Presently, there are more than one hundred ascoviral or iridoviral MCP sequences in databases. BLAST searches using these sequences failed to detect any similarities between CsIV virion proteins and ascoviral or iridoviral MCPs, or any other proteins [33]. To evaluate the possibility that homology between ichnovirus and ascovirus virion proteins may simply not be detectable by conventional Blastp searches, we used a different method, WAPAM (weighted automata pattern matching; [34]). The models were designed on the basis of a previous study [22] demonstrating that MCP encoded by ascovirus, iridovirus, phycodnavirus and asfarvirus genomes are related, and all contain 7 conserved domains separated by hinges of very variable size. We investigated these conserved domains further using hydrophobic cluster analysis (HCA, [35]). This analysis revealed that most conservation occurred at the level of hydrophobic residues, as expected for structural proteins (Additional file 3a and 3b). The size variability of the hinges between conserved domains and the conservation of hydrophobic residues might explain why BLAST searches using iridoviral and ascoviral MCP sequences have limited ability to detect MCP orthologs in phycodnavirus and asfarvirus genomes. We designed two syntactic models (see Materials and Methods), which together were able to specifically align all MCP sequences of the four virus families. Importantly, WAPAM aligned the CsIV ichnovirus P44 structural protein with both models. Complementary structural and HCA confirmed the presence of the seven conserved domains in this CsIV structural protein (Fig. 3a and Additional file 3c).

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