Abstract

While a number of studies have identified host factors that influence endosymbiont titer, little is known concerning environmental influences on titer. Here we examined nutrient impact on maternally transmitted Wolbachia endosymbionts in Drosophila. We demonstrate that Drosophila reared on sucrose- and yeast-enriched diets exhibit increased and reduced Wolbachia titers in oogenesis, respectively. The yeast-induced Wolbachia depletion is mediated in large part by the somatic TOR and insulin signaling pathways. Disrupting TORC1 with the small molecule rapamycin dramatically increases oocyte Wolbachia titer, whereas hyper-activating somatic TORC1 suppresses oocyte titer. Furthermore, genetic ablation of insulin-producing cells located in the Drosophila brain abolished the yeast impact on oocyte titer. Exposure to yeast-enriched diets altered Wolbachia nucleoid morphology in oogenesis. Furthermore, dietary yeast increased somatic Wolbachia titer overall, though not in the central nervous system. These findings highlight the interactions between Wolbachia and germline cells as strongly nutrient-sensitive, and implicate conserved host signaling pathways by which nutrients influence Wolbachia titer.

Highlights

  • Microbial endosymbionts have a profound impact on host metabolism and there are numerous examples in which microbes provide essential nutrients to the host [1,2,3,4,5,6,7,8,9,10,11,12,13,14]

  • We focused on Wolbachia endosymbionts that are carried naturally in the germ cells of fruit flies

  • We determined whether dietary nutrients affect the amount of Wolbachia bacteria carried by female flies

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Summary

Introduction

Microbial endosymbionts have a profound impact on host metabolism and there are numerous examples in which microbes provide essential nutrients to the host [1,2,3,4,5,6,7,8,9,10,11,12,13,14]. Researchers have observed that exposure to high levels of exogenous thiamine monophosphate suppresses the titer of Sodalis and Wigglesworthia endosymbionts in tsetse flies [15,16]. In this largely unexplored area, many outstanding questions remain: What are the host and endosymbiont metabolic and signaling pathways involved in nutrient sensing? In addition to its functional importance in Wolbachia transmission, the well-characterized molecular and cell biology of Drosophila oogenesis has provided considerable contextual information and experimental tools that can be applied to studies of Wolbachia-host interactions [18,26,27,28,29,30]

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