Regulation of Wolbachia ankyrin domain encoding genes in Drosophila gonads

Abstract

The maternally inherited obligatory intracellular bacterium Wolbachia is a reproductive parasite of many insect species. Wolbachia evades the host immune system, uses the mitotic apparatus to ensure infection of daughter cells, migrates through the host to the gonads and causes reproductive phenotypes, most commonly cytoplasmic incompatibility (CI), i.e. incompatibility of sperm from infected males and eggs from uninfected females. Due to the interconnected facts that Wolbachia is not ex vivo culturable and that no established transformation system exists, virtually nothing is known about Wolbachia-host interactions at the macromolecular level. Intriguingly, the Wolbachia genome codes for an unusually high number of ankyrin repeat (ANK) proteins. ANKs mediate protein-protein interactions in many different contexts. More common in eukaryotes, they also occur in prokaryotes. Some intracellular pathogenic bacteria export ANK effector proteins to the host cytoplasm. This makes the Wolbachia ANK genes candidates for mediating interactions with host cells. We quantified expression of ANK genes of Wolbachia strain wMel in adult gonads and detected host sex-specific regulation of two wMel ANK genes in the gonads in two different backgrounds. Regulation was tissue-specific and independent of host background. We further analyzed expression of their homologues in strains wAu and wRi and found regulation only in wAu. Regulation was tissue-specific and there was no correlation between regulation of these genes and the ability of a strain to induce CI.