Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior

Abstract

Animals host multi-species microbial communities (microbiomes) whose properties may result from inter-species interactions; however, current understanding of host-microbiome interactions derives mostly from studies in which elucidation of microbe-microbe interactions is difficult. In exploring how <i>Drosophila melanogaster</i> acquires its microbiome, we found that a microbial community influences <i>Drosophila</i> olfactory and egg-laying behaviors differently than individual members. <i>Drosophila</i> prefers a <i>Saccharomyces</i>-<i>Acetobacter</i> co-culture to the same microorganisms grown individually and then mixed, a response mainly due to the conserved olfactory receptor, <i>Or42b. Acetobacter</i> metabolism of <i>Saccharomyces-</i>derived ethanol was necessary, and acetate and its metabolic derivatives were sufficient, for co-culture preference. Preference correlated with three emergent co-culture properties: ethanol catabolism, a distinct volatile profile, and yeast population decline. Egg-laying preference provided a context-dependent fitness benefit to larvae. We describe a molecular mechanism by which a microbial community affects animal behavior. Our results support a model whereby emergent metabolites signal a beneficial multispecies microbiome.