Abstract

BackgroundIntracellular Wolbachia bacteria are obligate, maternally-inherited, endosymbionts found frequently in insects and other invertebrates. The success of Wolbachia can be attributed in part to an ability to alter host reproduction via mechanisms including cytoplasmic incompatibility (CI), parthenogenesis, feminization and male killing. Despite substantial scientific effort, the molecular mechanisms underlying the Wolbachia/host interaction are unknown.ResultsHere, an in vitro Wolbachia infection was generated in the Drosophila S2 cell line, and transcription profiles of infected and uninfected cells were compared by microarray. Differentially-expressed patterns related to reproduction, immune response and heat stress response are observed, including multiple genes that have been previously reported to be involved in the Wolbachia/host interaction. Subsequent in vivo characterization of differentially-expressed products in gonads demonstrates that Angiotensin Converting Enzyme (Ance) varies between Wolbachia infected and uninfected flies and that the variation occurs in a sex-specific manner. Consistent with expectations for the conserved CI mechanism, the observed Ance expression pattern is repeatable in different Drosophila species and with different Wolbachia types. To examine Ance involvement in the CI phenotype, compatible and incompatible crosses of Ance mutant flies were conducted. Significant differences are observed in the egg hatch rate resulting from incompatible crosses, providing support for additional experiments examining for an interaction of Ance with the CI mechanism.ConclusionWolbachia infection is shown to affect the expression of multiple host genes, including Ance. Evidence for potential Ance involvement in the CI mechanism is described, including the prior report of Ance in spermatid differentiation, Wolbachia-induced sex-specific effects on Ance expression and an Ance mutation effect on CI levels. The results support the use of Wolbachia infected cell cultures as an appropriate model for predicting in vivo host/Wolbachia interactions.

Highlights

  • Intracellular Wolbachia bacteria are obligate, maternally-inherited, endosymbionts found frequently in insects and other invertebrates

  • The ability of Wolbachia infections to spread and persist within this broad range of hosts can be attributed in part to its induction of multiple reproductive abnormalities including cytoplasmic incompatibility (CI), parthenogenesis, feminization and male killing

  • The results presented here show the S2 in vitro system to be a useful tool for examining the Wolbachia/ host interactions that affect host range and CI phenotype and for defining the host immune response to Wolbachia infection and Wolbachia immune evasion mechanisms

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Summary

Introduction

Intracellular Wolbachia bacteria are obligate, maternally-inherited, endosymbionts found frequently in insects and other invertebrates. The success of Wolbachia can be attributed in part to an ability to alter host reproduction via mechanisms including cytoplasmic incompatibility (CI), parthenogenesis, feminization and male killing. The molecular mechanisms underlying the Wolbachia/host interaction are unknown. The ability of Wolbachia infections to spread and persist within this broad range of hosts can be attributed in part to its induction of multiple reproductive abnormalities including cytoplasmic incompatibility (CI), parthenogenesis, feminization and male killing. Presence of T4SS in Wolbachia genome suggests a potential alteration of host cell expression as a means of facilitating its intracellular survival and dissemination, as observed for other intracellular bacteria [11]. A simplified model system, such as an in vitro Wolbachia infection within a well characterized cell culture, could potentially provide a useful tool for studying mechanisms of the Wolbachia/host interaction

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