The mosaic genome structure of the Wolbachia w Ri strain infecting Drosophila simulans

Abstract

The obligate intracellular bacterium Wolbachia pipientis infects around 20% of all insect species. It is maternally inherited and induces reproductive alterations of insect populations by male killing, feminization, parthenogenesis, or cytoplasmic incompatibility. Here, we present the 1,445,873-bp genome of W. pipientis strain w Ri that induces very strong cytoplasmic incompatibility in its natural host Drosophila simulans . A comparison with the previously sequenced genome of W. pipientis strain w Mel from Drosophila melanogaster identified 35 breakpoints associated with mobile elements and repeated sequences that are stable in Drosophila lines transinfected with w Ri. Additionally, 450 genes with orthologs in w Ri and w Mel were sequenced from the W. pipientis strain w Uni, responsible for the induction of parthenogenesis in the parasitoid wasp Muscidifurax uniraptor . The comparison of these A-group Wolbachia strains uncovered the most highly recombining intracellular bacterial genomes known to date. This was manifested in a 500-fold variation in sequence divergences at synonymous sites, with different genes and gene segments supporting different strain relationships. The substitution-frequency profile resembled that of Neisseria meningitidis , which is characterized by rampant intraspecies recombination, rather than that of Rickettsia , where genes mostly diverge by nucleotide substitutions. The data further revealed diversification of ankyrin repeat genes by short tandem duplications and provided examples of horizontal gene transfer across A- and B-group strains that infect D. simulans . These results suggest that the transmission dynamics of Wolbachia and the opportunity for coinfections have created a freely recombining intracellular bacterial community with mosaic genomes.