A Cellular Basis for Wolbachia Recruitment to the Host Germline

Abstract

Wolbachia are among the most widespread intracellular bacteria, carried by thousands of metazoan species. The success of Wolbachia is due to efficient vertical transmission by the host maternal germline. Some Wolbachia strains concentrate at the posterior of host oocytes, which promotes Wolbachia incorporation into posterior germ cells during embryogenesis. The molecular basis for this localization strategy is unknown. Here we report that the wMel Wolbachia strain relies upon a two-step mechanism for its posterior localization in oogenesis. The microtubule motor protein kinesin-1 transports wMel toward the oocyte posterior, then pole plasm mediates wMel anchorage to the posterior cortex. Trans-infection tests demonstrate that factors intrinsic to Wolbachia are responsible for directing posterior Wolbachia localization in oogenesis. These findings indicate that Wolbachia can direct the cellular machintery of host oocytes to promote germline-based bacterial transmission. This study also suggests parallels between Wolbachia localization mechanisms and those used by other intracellular pathogens. This study focuses on Wolbachia, a genus of intracellular bacteria carried by insect and nematode host species. It was recently shown that Wolbachia carried into the human body by the host nematode Onchocerca volvulus trigger an immune response that leads to African river blindness. Findings like these raise fundamental questions of how Wolbachia interact with host cells to perpetuate Wolbachia infection. Distinct from many pathogenic bacteria, Wolbachia are transmitted throughout host populations primarily from females to their offspring, similar to mitochondrial inheritance. The molecular basis for this transmission strategy is unclear. Here we show that Wolbachia transmission is aided by a complex mechanism in egg development. Our study suggests that Wolbachia are transported inside the egg as cargo of molecular motors that walk along microtubule filaments. This directs Wolbachia to the posterior of maturing eggs, thus placing Wolbachia at the site where reproductive cells form during embryogenesis and ensuring Wolbachia integration into those cells. Furthermore, both factors intrinsic to Wolbachia and host molecules specifying reproductive cell fates are necessary to maximize posterior concentration of Wolbachia in the egg. This suggests that Wolbachia manipulate conserved cellular machinery in egg development to direct their transmission to the next host generation.