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, 4 (7), e6397

Symbiotic Virus at the Evolutionary Intersection of Three Types of Large DNA Viruses; Iridoviruses, Ascoviruses, and Ichnoviruses

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Symbiotic Virus at the Evolutionary Intersection of Three Types of Large DNA Viruses; Iridoviruses, Ascoviruses, and Ichnoviruses

Yves Bigot et al. PLoS One.

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.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. 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).
Figure 2
Figure 2. Graphic presentation of DpAV4a ORF homologues in the genomes of three ascoviruses (SfAV1a, TnAV6a, and HvAV3e) and two invertebrate iridoviruses (Chilo iridovirus, CIV; and Mosquito iridovirus, MIV).
Figure 3
Figure 3. Synthesis of the evolutionary relationships among various genera of Mimiviridae (brown), Phycodnaviridae (green), Iridoviridae (invertebrate genera are in blue and vertebrate genera in dark blue), Ascoviridae (red), DpAV4a (purple) and ichnoviruses, Polydnaviridae (orange).
The name of the principal virus representative of each genus is indicated. A putative family of ascovirus-like particles (AV-lP) are in pink. This synthetic tree was determined from results obtained with the evolutionary analyses of the 28 core genes and the literature , , . Plain lines represent verified relationships. Dotted lines indicate evolutionary pathways between virus families that require further support for confirmation. Phylogenetic analyses of major capsid protein (MCP) sequences revealed that at least 3 groups (G1, G2, G3) occurred within the iridovirus genus. A hypothetical fourth one, G4, was used to support the putative origin of the Ascoviridae. Taxonomic details and full virus names in each virus family are available at: http://gicc.univ-tours.fr/collaborations/col_pics.php?connect=0&lang=fr or http://www.ncbi.nlm.nih.gov/ICTVdb/Ictv/fs_ascov.htm; http://www.ncbi.nlm.nih.gov/ICTVdb/Ictv/fs_irido.htm; http://www.ncbi.nlm.nih.gov/ICTVdb/ICTVdB/00.051.0.04.htm; http://www.ncbi.nlm.nih.gov/ICTVdb/Ictv/fs_mimiv.htm; http://www.ncbi.nlm.nih.gov/ICTVdb/Ictv/fs_asfar.htm; http://www.ncbi.nlm.nih.gov/ICTVdb/Ictv/fs_polyd.htm.

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