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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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Hypothetical mechanism for the integration and evolution of ascovirus genomes in endoparasitic wasps. Schematic representation of the three-step process of symbiogenesis, and DNA rearrangements that putatively occurred in the germ line of the wasp ancestors in the Banchinae and Campopleginae lineages, from the integration of an ascoviral genome to the proviral ichnoviral genome. Sequences that originate from the ascovirus are in blue, those of the wasp host and its chromosomes are in pink. Genes of ascoviral origin are surrounded by a thin black or white line, depending on their final chromosomal location. Two solutions can account for the final chromosomal organisation of the proviral ichnovirus genome, monolocus or multilocus, since this question is not fully understood in either wasp lineage. More complex alternatives to this three-step process might also be proposed and would involve, for example, the complete de novo creation of a mono or multi locus proviral genome from the recruitment by recombination or transposition of ascoviral and host genes located elsewhere in the wasp chromosomes. This model for the chromosomal organization of proviral DNA in polydnaviruses is consistent with data recently published [58].
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Figure 5: Hypothetical mechanism for the integration and evolution of ascovirus genomes in endoparasitic wasps. Schematic representation of the three-step process of symbiogenesis, and DNA rearrangements that putatively occurred in the germ line of the wasp ancestors in the Banchinae and Campopleginae lineages, from the integration of an ascoviral genome to the proviral ichnoviral genome. Sequences that originate from the ascovirus are in blue, those of the wasp host and its chromosomes are in pink. Genes of ascoviral origin are surrounded by a thin black or white line, depending on their final chromosomal location. Two solutions can account for the final chromosomal organisation of the proviral ichnovirus genome, monolocus or multilocus, since this question is not fully understood in either wasp lineage. More complex alternatives to this three-step process might also be proposed and would involve, for example, the complete de novo creation of a mono or multi locus proviral genome from the recruitment by recombination or transposition of ascoviral and host genes located elsewhere in the wasp chromosomes. This model for the chromosomal organization of proviral DNA in polydnaviruses is consistent with data recently published [58].

Mentions: Numerous cases of symbiogenesis between endocellular bacteria and a wide variety of eukaryotic hosts have been characterized. However, recent work has demonstrated that this evolutionary process was not restricted to bacteria. It also occurred between endocellular eukaryotes such as unicellular algae and fungal endophyte in plants [55,56]. Endosymbiogenesis was also proposed as the evolutionary mechanism that allowed some invertebrate viruses with a large double-stranded DNA genome related to the nudiviruses and the ascoviruses [22], to have led, respectively, to the origin of bracoviruses and ichnoviruses, which are currently recognized as forming two genera within the family Polydnaviridae. Although presently there is no definitive evidence ruling out the hypothesis that the resemblance between ichnovirus and ascovirus virions is only an evolutionary convergence, the genomic differences between ascovirus and ichnoviruses are in good agreement with the symbiogenetic hypothesis. Indeed, they match an evolutionary scenario of endosymbiogenesis during which, from a single integration event of symbiotic virus genome, viral genes were lost and/or translocated from the provirus to other chromosomal regions (Fig. 5). In parallel, host genes of interest for the wasp parasitoid were integrated and diversified by selection and gene duplication in the proviral DNA. In this scenario, the more ancient symbiogenesis, the rarer the traces of genes from viral origin in the ichnovirus genome would be. This constitutes a constraint that dramatically limits the possibility to investigate the evolutionary links between ascovirus and ichnovirus. Results of our analyses demonstrate that the situation is also complicated by the fact that lateral gene transfers unrelated to the origin of ichnoviruses cause important misleading background noise. Moreover, the scenario in Figure 5 is close to a previously proposed version [57], but is not consistent with results presented here, nor with recently accumulated knowledge on DNA transfer from organelles into the nucleus. Since endocellular environments favour lateral transfers between virus and wasp nucleus, it can be proposed that genes of virus origin that are involved in the ichnovirus biology were passively integrated in one or several loci, step by step over time, alone or through transfers of gene clusters, or even the entire viral genome. Since parasitoid wasps are able to vector different viruses [44,45], this second scenario opens the exciting possibility that virus genes involved in the ichnovirus biology might correspond to a gene patchwork resulting from transfers from viruses belonging to different NCLDV and non-NCLVD families. Because of the background noise due to lateral gene transfers found in these systems, elucidating the origins of ichnoviruses will be very time-consuming, requiring new accurate experimental approaches to generate more robust evidence. Sequencing wasp genomes to identify proteins of viral origin that are components of virions and involved in the assembly of these may well contribute to our understanding of how ichnoviruses and bracoviruses evolved from other insect DNA viruses.


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

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

Hypothetical mechanism for the integration and evolution of ascovirus genomes in endoparasitic wasps. Schematic representation of the three-step process of symbiogenesis, and DNA rearrangements that putatively occurred in the germ line of the wasp ancestors in the Banchinae and Campopleginae lineages, from the integration of an ascoviral genome to the proviral ichnoviral genome. Sequences that originate from the ascovirus are in blue, those of the wasp host and its chromosomes are in pink. Genes of ascoviral origin are surrounded by a thin black or white line, depending on their final chromosomal location. Two solutions can account for the final chromosomal organisation of the proviral ichnovirus genome, monolocus or multilocus, since this question is not fully understood in either wasp lineage. More complex alternatives to this three-step process might also be proposed and would involve, for example, the complete de novo creation of a mono or multi locus proviral genome from the recruitment by recombination or transposition of ascoviral and host genes located elsewhere in the wasp chromosomes. This model for the chromosomal organization of proviral DNA in polydnaviruses is consistent with data recently published [58].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Hypothetical mechanism for the integration and evolution of ascovirus genomes in endoparasitic wasps. Schematic representation of the three-step process of symbiogenesis, and DNA rearrangements that putatively occurred in the germ line of the wasp ancestors in the Banchinae and Campopleginae lineages, from the integration of an ascoviral genome to the proviral ichnoviral genome. Sequences that originate from the ascovirus are in blue, those of the wasp host and its chromosomes are in pink. Genes of ascoviral origin are surrounded by a thin black or white line, depending on their final chromosomal location. Two solutions can account for the final chromosomal organisation of the proviral ichnovirus genome, monolocus or multilocus, since this question is not fully understood in either wasp lineage. More complex alternatives to this three-step process might also be proposed and would involve, for example, the complete de novo creation of a mono or multi locus proviral genome from the recruitment by recombination or transposition of ascoviral and host genes located elsewhere in the wasp chromosomes. This model for the chromosomal organization of proviral DNA in polydnaviruses is consistent with data recently published [58].
Mentions: Numerous cases of symbiogenesis between endocellular bacteria and a wide variety of eukaryotic hosts have been characterized. However, recent work has demonstrated that this evolutionary process was not restricted to bacteria. It also occurred between endocellular eukaryotes such as unicellular algae and fungal endophyte in plants [55,56]. Endosymbiogenesis was also proposed as the evolutionary mechanism that allowed some invertebrate viruses with a large double-stranded DNA genome related to the nudiviruses and the ascoviruses [22], to have led, respectively, to the origin of bracoviruses and ichnoviruses, which are currently recognized as forming two genera within the family Polydnaviridae. Although presently there is no definitive evidence ruling out the hypothesis that the resemblance between ichnovirus and ascovirus virions is only an evolutionary convergence, the genomic differences between ascovirus and ichnoviruses are in good agreement with the symbiogenetic hypothesis. Indeed, they match an evolutionary scenario of endosymbiogenesis during which, from a single integration event of symbiotic virus genome, viral genes were lost and/or translocated from the provirus to other chromosomal regions (Fig. 5). In parallel, host genes of interest for the wasp parasitoid were integrated and diversified by selection and gene duplication in the proviral DNA. In this scenario, the more ancient symbiogenesis, the rarer the traces of genes from viral origin in the ichnovirus genome would be. This constitutes a constraint that dramatically limits the possibility to investigate the evolutionary links between ascovirus and ichnovirus. Results of our analyses demonstrate that the situation is also complicated by the fact that lateral gene transfers unrelated to the origin of ichnoviruses cause important misleading background noise. Moreover, the scenario in Figure 5 is close to a previously proposed version [57], but is not consistent with results presented here, nor with recently accumulated knowledge on DNA transfer from organelles into the nucleus. Since endocellular environments favour lateral transfers between virus and wasp nucleus, it can be proposed that genes of virus origin that are involved in the ichnovirus biology were passively integrated in one or several loci, step by step over time, alone or through transfers of gene clusters, or even the entire viral genome. Since parasitoid wasps are able to vector different viruses [44,45], this second scenario opens the exciting possibility that virus genes involved in the ichnovirus biology might correspond to a gene patchwork resulting from transfers from viruses belonging to different NCLDV and non-NCLVD families. Because of the background noise due to lateral gene transfers found in these systems, elucidating the origins of ichnoviruses will be very time-consuming, requiring new accurate experimental approaches to generate more robust evidence. Sequencing wasp genomes to identify proteins of viral origin that are components of virions and involved in the assembly of these may well contribute to our understanding of how ichnoviruses and bracoviruses evolved from other insect DNA viruses.

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