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Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.

Bigot Y, Renault S, Nicolas J, Moundras C, Demattei MV, Samain S, Bideshi DK, Federici BA - PLoS ONE (2009)

Bottom Line: Analyses of core DpAV4a genes confirmed that ascoviruses and iridoviruses are evolutionary related.Our analyses also revealed that DpAV4a shared more core genes with CIV than with other ascoviruses and iridoviruses, providing additional evidence that DpAV4a represents a separate lineage.Given the differences in the biology of the various iridoviruses and ascoviruses studied, these results provide an interesting model for how viruses of different families evolved from one another.

View Article: PubMed Central - PubMed

Affiliation: Génétique, Immmunothérapie, Chimie et Cancer, UMR CNRS 6239, Université François Rabelais de Tours, UFR des Sciences et Techniques, Parc de Grandmont, Tours, France. bigot@univ-tours.fr

ABSTRACT

Background: The ascovirus, DpAV4a (family Ascoviridae), is a symbiotic virus that markedly increases the fitness of its vector, the parasitic ichneumonid wasp, Diadromus puchellus, by increasing survival of wasp eggs and larvae in their lepidopteran host, Acrolepiopsis assectella. Previous phylogenetic studies have indicated that DpAV4a is related to the pathogenic ascoviruses, such as the Spodoptera frugiperda ascovirus 1a (SfAV1a) and the lepidopteran iridovirus (family Iridoviridae), Chilo iridescent virus (CIV), and is also likely related to the ancestral source of certain ichnoviruses (family Polydnaviridae).

Methodology/principal findings: To clarify the evolutionary relationships of these large double-stranded DNA viruses, we sequenced the genome of DpAV4a and undertook phylogenetic analyses of the above viruses and others, including iridoviruses pathogenic to vertebrates. The DpAV4a genome consisted of 119,343 bp and contained at least 119 open reading frames (ORFs), the analysis of which confirmed the relatedness of this virus to iridoviruses and other ascoviruses.

Conclusions: Analyses of core DpAV4a genes confirmed that ascoviruses and iridoviruses are evolutionary related. Nevertheless, our results suggested that the symbiotic DpAV4a had a separate origin in the iridoviruses from the pathogenic ascoviruses, and that these two types shared parallel evolutionary paths, which converged with respect to virion structure (icosahedral to bacilliform), genome configuration (linear to circular), and cytopathology (plasmalemma blebbing to virion-containing vesicles). Our analyses also revealed that DpAV4a shared more core genes with CIV than with other ascoviruses and iridoviruses, providing additional evidence that DpAV4a represents a separate lineage. Given the differences in the biology of the various iridoviruses and ascoviruses studied, these results provide an interesting model for how viruses of different families evolved from one another.

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Schematic illustration of the organization of the Diadromus pulchellus ascovirus 4a (DpAV4a) genome.Predicted ORFs are indicated by their location, orientation, and putative size. White arrows represent ORFs on the forward strand, whereas black arrows identify those on the reverse strand. ORFs corresponding to members of repeated protein families are light orange for the BRO-like proteins, green for the metallo-hydrolases, and purple for the ABC-type transport system permease. ORFs encoding peptides present in TnAV2a and SfAV1a virions are light blue. The DpAV4a genomic map was constructed using Vector NTI (Invitrogene).
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pone-0006397-g001: Schematic illustration of the organization of the Diadromus pulchellus ascovirus 4a (DpAV4a) genome.Predicted ORFs are indicated by their location, orientation, and putative size. White arrows represent ORFs on the forward strand, whereas black arrows identify those on the reverse strand. ORFs corresponding to members of repeated protein families are light orange for the BRO-like proteins, green for the metallo-hydrolases, and purple for the ABC-type transport system permease. ORFs encoding peptides present in TnAV2a and SfAV1a virions are light blue. The DpAV4a genomic map was constructed using Vector NTI (Invitrogene).

Mentions: A total of 433 open reading frames (ORFs) with a methionine start codon and a minimum protein size of 50 amino acids were identified in the DpAV4a genome. Among these, 119 ORFs with no or minimal overlap (≤150 nt) were assumed to encode putative proteins (Fig. 1; Fig. S2). In agreement with previous sequencing studies of ascovirus genomes [15]–[17], the A of the ATG start codon of the ORF encoding the DNA polymerase B was arbitrarily assigned position 1 for the DpAV4a genome. The predicted ORFs were not distributed equally on both strands; 71 were in forward orientation whereas 48 were in the reverse orientation, with many of these being arranged in unidirectional gene clusters. ORFs represent 88.5% of the genome with an average density of one gene per 887 bp. We detected a linear relationship between the ORF number and genome size among most ascovirus and iridovirus genomes (Fig. S3; R2 = 0.757), with the exceptions being the genomes of MIV [19] and SfAV1a [15]. In MIV, this was due primarily to the presence of fifteen large repeats representing about 20% of its genome. In SfAV1a, this is due to the presence of (a) two large non-coding inverted repeats (7.4% of the genome), (b) an ORF65bis (Fig. S4a; [6]), and (c) to 61 overlapping ORFs described previously [15], named ORF A to OOO (Fig. S4b), but not referenced in Genebank. We found that 26 of the SfAV1a ORFs were present in the HvAV3e genome, and 10 of the same in the TnAV6a genome. In the DpAV4a genome, we determined that the ORF023 is a homologue of the SfAV1a ORF R, and that ORFs 056 and 057 are homologues of the SfAV1a ORF P. Interestingly, we found no homologue for each of these 61 SfAV1a ORFs among the ORFs contained in vertebrate and invertebrate iridovirus genomes. This suggested, therefore, that these 26 SfAV1a ORFs were characteristic of ascovirus genomes. Taking into account these data and errata (Fig. S4c), we adjusted the genomes sizes and ORF number of MIV and SfAV1a accordingly, which yielded a very significant linear correlation (R2 = 0.9265) between ORF number and the genome size of these two viruses (Fig. S3).


Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.

Bigot Y, Renault S, Nicolas J, Moundras C, Demattei MV, Samain S, Bideshi DK, Federici BA - PLoS ONE (2009)

Schematic illustration of the organization of the Diadromus pulchellus ascovirus 4a (DpAV4a) genome.Predicted ORFs are indicated by their location, orientation, and putative size. White arrows represent ORFs on the forward strand, whereas black arrows identify those on the reverse strand. ORFs corresponding to members of repeated protein families are light orange for the BRO-like proteins, green for the metallo-hydrolases, and purple for the ABC-type transport system permease. ORFs encoding peptides present in TnAV2a and SfAV1a virions are light blue. The DpAV4a genomic map was constructed using Vector NTI (Invitrogene).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2712680&req=5

pone-0006397-g001: Schematic illustration of the organization of the Diadromus pulchellus ascovirus 4a (DpAV4a) genome.Predicted ORFs are indicated by their location, orientation, and putative size. White arrows represent ORFs on the forward strand, whereas black arrows identify those on the reverse strand. ORFs corresponding to members of repeated protein families are light orange for the BRO-like proteins, green for the metallo-hydrolases, and purple for the ABC-type transport system permease. ORFs encoding peptides present in TnAV2a and SfAV1a virions are light blue. The DpAV4a genomic map was constructed using Vector NTI (Invitrogene).
Mentions: A total of 433 open reading frames (ORFs) with a methionine start codon and a minimum protein size of 50 amino acids were identified in the DpAV4a genome. Among these, 119 ORFs with no or minimal overlap (≤150 nt) were assumed to encode putative proteins (Fig. 1; Fig. S2). In agreement with previous sequencing studies of ascovirus genomes [15]–[17], the A of the ATG start codon of the ORF encoding the DNA polymerase B was arbitrarily assigned position 1 for the DpAV4a genome. The predicted ORFs were not distributed equally on both strands; 71 were in forward orientation whereas 48 were in the reverse orientation, with many of these being arranged in unidirectional gene clusters. ORFs represent 88.5% of the genome with an average density of one gene per 887 bp. We detected a linear relationship between the ORF number and genome size among most ascovirus and iridovirus genomes (Fig. S3; R2 = 0.757), with the exceptions being the genomes of MIV [19] and SfAV1a [15]. In MIV, this was due primarily to the presence of fifteen large repeats representing about 20% of its genome. In SfAV1a, this is due to the presence of (a) two large non-coding inverted repeats (7.4% of the genome), (b) an ORF65bis (Fig. S4a; [6]), and (c) to 61 overlapping ORFs described previously [15], named ORF A to OOO (Fig. S4b), but not referenced in Genebank. We found that 26 of the SfAV1a ORFs were present in the HvAV3e genome, and 10 of the same in the TnAV6a genome. In the DpAV4a genome, we determined that the ORF023 is a homologue of the SfAV1a ORF R, and that ORFs 056 and 057 are homologues of the SfAV1a ORF P. Interestingly, we found no homologue for each of these 61 SfAV1a ORFs among the ORFs contained in vertebrate and invertebrate iridovirus genomes. This suggested, therefore, that these 26 SfAV1a ORFs were characteristic of ascovirus genomes. Taking into account these data and errata (Fig. S4c), we adjusted the genomes sizes and ORF number of MIV and SfAV1a accordingly, which yielded a very significant linear correlation (R2 = 0.9265) between ORF number and the genome size of these two viruses (Fig. S3).

Bottom Line: Analyses of core DpAV4a genes confirmed that ascoviruses and iridoviruses are evolutionary related.Our analyses also revealed that DpAV4a shared more core genes with CIV than with other ascoviruses and iridoviruses, providing additional evidence that DpAV4a represents a separate lineage.Given the differences in the biology of the various iridoviruses and ascoviruses studied, these results provide an interesting model for how viruses of different families evolved from one another.

View Article: PubMed Central - PubMed

Affiliation: Génétique, Immmunothérapie, Chimie et Cancer, UMR CNRS 6239, Université François Rabelais de Tours, UFR des Sciences et Techniques, Parc de Grandmont, Tours, France. bigot@univ-tours.fr

ABSTRACT

Background: The ascovirus, DpAV4a (family Ascoviridae), is a symbiotic virus that markedly increases the fitness of its vector, the parasitic ichneumonid wasp, Diadromus puchellus, by increasing survival of wasp eggs and larvae in their lepidopteran host, Acrolepiopsis assectella. Previous phylogenetic studies have indicated that DpAV4a is related to the pathogenic ascoviruses, such as the Spodoptera frugiperda ascovirus 1a (SfAV1a) and the lepidopteran iridovirus (family Iridoviridae), Chilo iridescent virus (CIV), and is also likely related to the ancestral source of certain ichnoviruses (family Polydnaviridae).

Methodology/principal findings: To clarify the evolutionary relationships of these large double-stranded DNA viruses, we sequenced the genome of DpAV4a and undertook phylogenetic analyses of the above viruses and others, including iridoviruses pathogenic to vertebrates. The DpAV4a genome consisted of 119,343 bp and contained at least 119 open reading frames (ORFs), the analysis of which confirmed the relatedness of this virus to iridoviruses and other ascoviruses.

Conclusions: Analyses of core DpAV4a genes confirmed that ascoviruses and iridoviruses are evolutionary related. Nevertheless, our results suggested that the symbiotic DpAV4a had a separate origin in the iridoviruses from the pathogenic ascoviruses, and that these two types shared parallel evolutionary paths, which converged with respect to virion structure (icosahedral to bacilliform), genome configuration (linear to circular), and cytopathology (plasmalemma blebbing to virion-containing vesicles). Our analyses also revealed that DpAV4a shared more core genes with CIV than with other ascoviruses and iridoviruses, providing additional evidence that DpAV4a represents a separate lineage. Given the differences in the biology of the various iridoviruses and ascoviruses studied, these results provide an interesting model for how viruses of different families evolved from one another.

Show MeSH
Related in: MedlinePlus