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

Abstract

BackgroundThe 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 FindingsTo 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.ConclusionsAnalyses 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.

Genomic Sequence of Heliothis virescens Ascovirus 3g Isolated from Spodoptera exigua

“…DNA sequence analysis showed that HvAV-3g has a genome size of 199,721 bp, which is the largest among all the reported ascovirus genomes to date (2,3,5,14). The HvAV-3g genome has a GϩC content of 45.9%, which is similar to that of HvAV-3e (45.8%) but dissimilar to that of SfAV-1a (49.2%), TnAV-2c (35.4%) and DpAV-4a (49.66%) (2,3,5,14).…”

“…The HvAV-3g genome has a GϩC content of 45.9%, which is similar to that of HvAV-3e (45.8%) but dissimilar to that of SfAV-1a (49.2%), TnAV-2c (35.4%) and DpAV-4a (49.66%) (2,3,5,14). There are 194 open reading frames (ORFs) encoding predicted proteins of more than 50 amino acids.…”

An Ascovirus-Encoded RNase III Autoregulates Its Expression and Suppresses RNA Interference-Mediated Gene Silencing

“…Ascoviruses (AVs) are pathogenic to lepidopteran insects at larval and pupal stages (6). After infection, the host cell morphology resembles that of apoptotic cells producing vesicles that look like apoptotic bodies through which virions are disseminated (5).…”

“…The virions can be transmitted mechanically by the ovipositor of female parasitic wasps between caterpillars (15). Genome sequences (119-to 187-kbp dsDNA) of four recognized AV species, Spodoptera frugiperda AV (SfAV-1), Trichoplusia ni AV (TnAV-2), Heliothis virescens AV (HvAV-3), and Diadromus pulchellus AV (DpAV-4) are now available (1,4,6,30). Phylogenetic studies suggest that AVs may have evolved from iridoviruses that infect lepidopteran larvae (15,29).…”

Functional Analysis of a Cellular MicroRNA in Insect Host-Ascovirus Interaction

“…These viruses possess a single circular double-stranded DNA genome ranging from 119 to 186 kbp and is encapsidated in virions of allantoid to bacilliform shapes (10). There are four recognized AV species, Spodoptera frugiperda AV (SfAV-1), Trichoplusia ni AV (TnAV-2), Heliothis virescens AV (HvAV-3), and Diadromus pulchellus AV (DpAV-4), and their complete genome sequences now are available (1)(2)(3)31). AVs are transmitted by wasp vectors, and their association with the vector could either be antagonistic (SfAV-1, TnAV-2, and HvAV-3) or mutualistic (DpAV-4) (4).…”