Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior

• Main Authors: Caleb N Fischer, Eric P Trautman, Jason M Crawford, Eric V Stabb, Jo Handelsman, Nichole A Broderick
• Format: Article
• Language: English
• Published: eLife Sciences Publications Ltd 2017-01-01
• Series: eLife
• Subjects: microbiota; host-microbe interactions; olfaction; metabolism; microbe-microbe interactions
• Online Access: https://elifesciences.org/articles/18855

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 Drosophila melanogaster acquires its microbiome, we found that a microbial community influences Drosophila olfactory and egg-laying behaviors differently than individual members. Drosophila prefers a Saccharomyces-Acetobacter co-culture to the same microorganisms grown individually and then mixed, a response mainly due to the conserved olfactory receptor, Or42b. Acetobacter metabolism of Saccharomyces-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.