Polydnavirus genomes reflect their dual roles as mutualists and pathogens.

Symbionts often exhibit significant reductions in genome complexity while pathogens often exhibit increased complexity through acquisition and diversification of virulence determinants. A few organisms have evolved complex life cycles in which they interact as symbionts with one host and pathogens with another. How the predicted and opposing influences of symbiosis and pathogenesis affect genome evolution in such instances, however, is unclear. The Polydnaviridae is a family of double-stranded (ds) DNA viruses associated with parasitoid wasps that parasitize other insects. Polydnaviruses (PDVs) only replicate in wasps but infect and cause severe disease in parasitized hosts. This disease is essential for survival of the parasitoid's offspring. Thus, a true mutualism exists between PDVs and wasps as viral transmission depends on parasitoid survival and parasitoid survival depends on viral infection of the wasp's host. To investigate how life cycle and ancestry affect PDVs, we compared the genomes of Campoletis sonorensis ichnovirus (CsIV) and Microplitis demolitor bracovirus (MdBV). CsIV and MdBV have no direct common ancestor, yet their encapsidated genomes share several features including segmentation, diversification of virulence genes into families, and the absence of genes required for replication. In contrast, CsIV and MdBV share few genes expressed in parasitized hosts. We conclude that the similar organizational features of PDV genomes reflect their shared life cycle but that PDVs associated with ichneumonid and braconid wasps have likely evolved different strategies to cause disease in the wasp's host and promote parasitoid survival.

Characterization of Campoletis sonorensis ichnovirus unique segment B and excision locus structure.

Polydnaviruses (PDVs) are segmented, symbiotic, double-stranded DNA viruses that are vertically transmitted as proviruses within the genomes of some parasitoid Hymenoptera. The PDV associated with the ichneumonid wasp Campoletis sonorensis (CsIV) consists of 24 non-redundant DNA segments varying in size from approximately 6 to 20 kbp. CsIV segment B, one of the smallest genome segments, was sequenced and the excision sites of the proviral segment were characterized. The segment B sequence was 83.2% non-coding with only two open reading frames (ORFs). Some non-coding sequences have similarities to database sequences and were likely pseudogenic, but most were unrelated to known nucleic acid or predicted protein sequences. One ORF, BHv0.9, encodes a member of the rep gene family and was expressed only in parasitized insects while transcription of the other ORF could not be detected. Previously, a third region of the segment was shown to hybridize to 0.6 and 1.2 kb poly A+ RNAs from female wasps during virus replication (Theilmann and Summers, 1988) but this region did not have an identifiable ORF in the determined sequence. In contrast to CsIV segment W, segment B had little repetitive sequence. The segment B proviral integration locus contains a 59 bp direct imperfect repeat. Further analyses of this integration locus demonstrated that segment B was excised from wasp genomic DNA with flanking sequences at the integration site rejoined after segment excision. The segment B "excision locus" retained one of the two copies of the 59 bp repeat sequence with the other repeat present in the excised segment. The data indicate that Ichnovirus segments have distinctive characteristics possibly reflecting functional co-evolution between the wasp and individual types of polydnavirus segments.