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Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior

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 D...

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Autores principales: Fischer, Caleb N, Trautman, Eric P, Crawford, Jason M, Stabb, Eric V, Handelsman, Jo, Broderick, Nichole A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5222558/
https://www.ncbi.nlm.nih.gov/pubmed/28068220
http://dx.doi.org/10.7554/eLife.18855
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author Fischer, Caleb N
Trautman, Eric P
Crawford, Jason M
Stabb, Eric V
Handelsman, Jo
Broderick, Nichole A
author_facet Fischer, Caleb N
Trautman, Eric P
Crawford, Jason M
Stabb, Eric V
Handelsman, Jo
Broderick, Nichole A
author_sort Fischer, Caleb N
collection PubMed
description 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. DOI: http://dx.doi.org/10.7554/eLife.18855.001
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spelling pubmed-52225582017-01-11 Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior Fischer, Caleb N Trautman, Eric P Crawford, Jason M Stabb, Eric V Handelsman, Jo Broderick, Nichole A eLife Ecology 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. DOI: http://dx.doi.org/10.7554/eLife.18855.001 eLife Sciences Publications, Ltd 2017-01-09 /pmc/articles/PMC5222558/ /pubmed/28068220 http://dx.doi.org/10.7554/eLife.18855 Text en © 2017, Fischer et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Ecology
Fischer, Caleb N
Trautman, Eric P
Crawford, Jason M
Stabb, Eric V
Handelsman, Jo
Broderick, Nichole A
Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior
title Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior
title_full Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior
title_fullStr Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior
title_full_unstemmed Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior
title_short Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior
title_sort metabolite exchange between microbiome members produces compounds that influence drosophila behavior
topic Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5222558/
https://www.ncbi.nlm.nih.gov/pubmed/28068220
http://dx.doi.org/10.7554/eLife.18855
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