Abstract

Unlike vertically transmitted endosymbionts, which have broad effects on their host's germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line. Here we provide evidence supporting the influence of these gut bacteria on the germ line of Drosophila melanogaster. Removal of the gut bacteria represses oogenesis, expedites maternal-to-zygotic-transition in the offspring and unmasks hidden phenotypic variation in mutants. We further show that the main impact on oogenesis is linked to the lack of gut Acetobacter species, and we identify the Drosophila Aldehyde dehydrogenase (Aldh) gene as an apparent mediator of repressed oogenesis in Acetobacter-depleted flies. The finding of interactions between the gut microbiota and the germ line has implications for reproduction, developmental robustness and adaptation.

Highlights

  • Unlike vertically transmitted endosymbionts, which have broad effects on their host’s germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line

  • We investigated the influence of extracellular gut bacteria on reproductive capacity of the fly by eliminating the bacteria using egg dechorionation and sterilization[18]

  • Similar results were observed in a Wolbachia-free fly strain (Oregon R), indicating that the repression of oogenesis and reproduction in bacterial-depleted flies is independent of Wolbachia (Supplementary Fig. 1A,B)

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Summary

Introduction

Unlike vertically transmitted endosymbionts, which have broad effects on their host’s germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line. We provide evidence supporting the influence of these gut bacteria on the germ line of Drosophila melanogaster. Many lab stocks are infected with the endosymbiont Wolbachia pipientis[20,21], which is transmitted vertically within the germ line and has been implicated in manipulation of reproduction in many Drosophila species[22,23,24]. We provide multiple lines of evidence supporting the influence of extracellular gut bacteria (primarily gut Acetobacter) on oogenesis and subsequent embryonic development in the following generation. We find that removal of extracellular gut bacteria in one generation leads to phenotypic unmasking of genetic mutations and reduces antibiotic tolerance in the generation These findings uncover a hitherto unrealized dimension of gut microbiome–germline interactions

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