title: Metabolite exchange between microbiome members produces compounds that influenceDrosophilabehavior.
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 howDrosophila melanogasteracquires its microbiome, we found that a microbial community influencesDrosophilaolfactory and egg-laying behaviors differently than individual members.Drosophilaprefers aSaccharomyces-Acetobacterco-culture to the same microorganisms grown individually and then mixed, a response mainly due to the conserved olfactory receptor,Or42b. Acetobactermetabolism ofSaccharomyces-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.
authors.affiliation: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States.
authors.forename: Caleb N
authors.identifier: 0000-0003-4223-8511
authors.initials: CN
authors.lastname: Fischer
authors.affiliation: Department of Chemistry, Yale University, New Haven, United States.
authors.forename: Eric P
authors.initials: EP
authors.lastname: Trautman
authors.affiliation: Department of Chemistry, Yale University, New Haven, United States.
authors.forename: Jason M
authors.identifier: 0000-0002-7583-1242
authors.initials: JM
authors.lastname: Crawford
authors.affiliation: Department of Microbiology, University of Georgia, Athens, United States.
authors.forename: Eric V
authors.initials: EV
authors.lastname: Stabb
authors.affiliation: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States.
authors.forename: Jo
authors.initials: J
authors.lastname: Handelsman
authors.affiliation: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States.|Department of Molecular and Cell Biology, University of Connecticut, Storrs, United States.|Institute for Systems Genomics, University of Connecticut, Storrs, United States.
authors.forename: Nichole A
authors.identifier: 0000-0002-6830-9456
authors.initials: NA
authors.lastname: Broderick
mesh_terms: D019342:Acetic Acid / Q000378:metabolism; D000091:Acetobacter / Q000378:metabolism*; D000818:Animals; D001522:Behavior, Animal / Q000187:drug effects*; D004331:Drosophila melanogaster / Q000187:drug effects* / Q000502:physiology*; D000431:Ethanol / Q000378:metabolism; D064307:Microbiota; D012440:Saccharomyces / Q000378:metabolism*; D055549:Volatile Organic Compounds / Q000378:metabolism
chemical_list: D055549:Volatile Organic Compounds; D000431:Ethanol; D019342:Acetic Acid
keywords: D. melanogaster; S. cerevisiae; ecology; host-microbe interactions; infectious disease; metabolism; microbe-microbe interactions; microbiology; microbiota; olfaction