Polydnavirus genomes reflect their dual roles as mutualists and pathogens

Abstract

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.

Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the mothPseudoplusia includens

“…The first is that post-critical weight larvae are refractory to infection or that insufficient time exists after infection of post-critical weight larvae for the effects of viral expression to block pupation. We think this unlikely given prior analyses of the fully sequenced MdBV genome which indicate transcription of most viral genes begins within 2 h of infection and continues near steady state for multiple days thereafter with no differences between last instar hosts infected pre-and post-critical weight (Strand et al, 1992;Strand, 1994;Webb et al, 2006;Pruijssers and Strand, 2007; (and M.R.S. and M. H. Beck, unpublished).…”

“…In summary, our results argue that M. demolitor and likely several other PDV-carrying wasps inhibit host pupation by altering feeding behavior and metabolic physiology rather than directly altering hormone synthesis or release. MdBV encodes more than 60 predicted open reading frames which include a mixture of single copy genes and structurally related genes that form multimember families (Webb and Strand, 2005;Webb et al, 2006;Strand, 2008). A key priority is to determine whether any MdBV gene products function as growth inhibitors.…”

Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa

“…The Aquarium Control and DOC samples contained a large fraction of sequences similar to ssDNA viruses from plants (white bars) such as geminiviruses and nanoviruses (39). Invertebrate infecting viruses (black bars) were also abundant (Ͼ60%) within the time zero library and were mostly similar to the baculoviruses and polydnaviruses, 2 viral families that predominantly infect arthropods (40)(41)(42). However, a caveat to this analysis is that the predicted host range is biased by the larger number of completed vertebrateassociated viral genomes.…”

Exogenous JH and ecdysteroid applications alter initiation of polydnaviral replication in an endoparasitoid wasp, Cotesia plutellae (Braconidae: Hymenoptera)

“…For PDV replication, including CpBV, a viral DNA polymerase or any associated factor(s) that use host DNA polymerase are necessary. However, no PDV-possessing DNA polymerase has been identified since its gene is not likely to be encapsulated in viral particles (32). Current approaches for identifying PDV genomes using ovarian EST or analysis of BAC clones containing PDV segments clearly suggest that viral coat protein genes, which are not encapsulated, are actively expressed during viral replication (33,34).…”