The Gut Microbiome Attenuates the Adaptation of a Reproductive Endosymbiont

Abstract

Holobionts contain spatially separated microbes whose interorgan effects are a neglected source of potential, functional variation. Here we show the extracellular gut microbiome modulates the transcriptome and adaptation of the endosymbiont Wolbachia in Drosophila melanogaster testes. Gut bacteria suppress cytoplasmic incompatibility (CI), a sperm-egg lethality trait, by altering endosymbiont pathogenicity gene expression. Transgenic assays identify the enchancer of cytoplasmic incompatibility gene eci as causal to the variation. Restoring the gut microbiome in laboratory and wild-caught, germ-free flies recapitulates CI attenuation and shifts host fitness. Intact holobionts sustain higher densities of the two symbiont types versus isolated rearing, revealing a synergistic, replication interaction between the symbiont classes. The gut-germline axis on symbiont functions has far-reaching implications for the study of holobiont trait variation.