Widespread Genome Reorganization of an Obligate Virus Mutualist

Abstract

The family Polydnaviridae is of interest because it provides the best example of viruses that have evolved a mutualistic association with their animal hosts. Polydnaviruses in the genus Bracovirus are strictly associated with parasitoid wasps in the family Braconidae, and evolved ∼100 million years ago from a nudivirus. Each wasp species relies on its associated bracovirus to parasitize hosts, while each bracovirus relies on its wasp for vertical transmission. Prior studies establish that bracovirus genomes consist of proviral segments and nudivirus-like replication genes, but how these components are organized in the genomes of wasps is unknown. Here, we sequenced the genome of the wasp Microplitis demolitor to characterize the proviral genome of M. demolitor bracovirus (MdBV). Unlike nudiviruses, bracoviruses produce virions that package multiple circular, double-stranded DNAs. DNA segments packaged into MdBV virions resided in eight dispersed loci in the M. demolitor genome. Each proviral segment was bounded by homologous motifs that guide processing to form mature viral DNAs. Rapid evolution of proviral segments obscured homology between other bracovirus-carrying wasps and MdBV. However, some domains flanking MdBV proviral loci were shared with other species. All MdBV genes previously identified to encode proteins required for replication were identified. Some of these genes resided in a multigene cluster but others, including subunits of the RNA polymerase that transcribes structural genes and integrases that process proviral segments, were widely dispersed in the M. demolitor genome. Overall, our results indicate that genome dispersal is a key feature in the evolution of bracoviruses into mutualists.

The Genome of the Nucleopolyhedrosis-Causing Virus from Tipula oleracea Sheds New Light on the Nudiviridae Family

“…*, genes belonging to the nudiviral cluster identified within C. congregata or M. demolitor wasp genomes (37,38,67). Direct repeat (dr) region position and name are indicated as boxes (see also (44).…”

“…Likewise, a hypothetical protein at the locus tag K425_450 of the nudiviral cluster of the braconid wasp M. demolitor was identified as homologous to ToNV ORF027 and GbNV ORF19, and Cc50C22.5 as homologous to PmNV ORF87. However, so far no ToNV homologs have been identified for HzNVorf94-like or 35a (37,(65)(66)(67) or for the three newly identified MdBV putative nudiviral genes (locus tags K425_456, K425_459, and K425_461) (67). ToNV thus appears as an exogenous nudivirus most closely related to the ancestral nudivirus, whose genome integrated into the ancestor of the braconid wasps, thus producing bracoviruses.…”

“…DiNV, Drosophila innubia NV; SfMNPV, Spodoptera frugiperda MNPV; ApNPV, Antheraea pernyi NPV; MacoNPV, Mamestra configurata NPV; PsunGV, Pseudaletia unipuncta granulovirus; PiraGV, Pieris rapae granulovirus; ChocNPV, Choristoneura occidentalis alphabaculovirus (see Table 1 for definitions of other virus name abbreviations). *, belongs to the nudiviral cluster characterized within C. congregata or M. demolitor wasp genomes (37,38,67); §, sequence similarity identified using local BLASTP or BLAST2 sequence comparison against a restricted protein database and global alignment for homolog confirmation (MAFFT under Geneious); $, sequence similarity identified using probabilistic methods (HMMER); ϩ, gene present;°, gene not predicted in the genome of some nudiviruses but present; #, Rohrmann et al, 1981 (24). Boxes surrounding multiple ORF numbers indicate regions of microsynteny between ToNV and the other nudivirus genomes.…”

“…Bracoviruses evolved from the integration of a nudivirus in the genome of an ancestral parasitic wasp (37,65). The genome of the wasps Cotesia congregata and Microplitis demolitor have retained a locus, comprising at least 10 genes from the original viral genome, termed the nudiviral cluster (37,66,67). ToNV displayed 12 of these nudivirus-like genes present in bracoviruses, although dispersed within its genome rather than as a cluster ( Fig.…”

Microplitis demolitor Bracovirus Proviral Loci and Clustered Replication Genes Exhibit Distinct DNA Amplification Patterns during Replication

“…The second component consists primarily of genes related to nudivirus and baculovirus core genes. These genes are transcribed in calyx cells during replication and are essential for virion formation, but none reside on DNAs that are packaged into nucleocapsids (2,11,12). Together, these features underlie the fact that BV virions are replication defective yet package DNAs that have essential functions in parasitism.…”