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...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-01-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/18855 |
| _version_ | 1811181083979415552 |
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| author | Caleb N Fischer Eric P Trautman Jason M Crawford Eric V Stabb Jo Handelsman Nichole A Broderick |
| author_facet | Caleb N Fischer Eric P Trautman Jason M Crawford Eric V Stabb Jo Handelsman Nichole A Broderick |
| author_sort | Caleb N Fischer |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T09:13:51Z |
| format | Article |
| id | doaj.art-5a2250144aec42779b061ff4aceea4e3 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:13:51Z |
| publishDate | 2017-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-5a2250144aec42779b061ff4aceea4e32022-12-22T04:32:26ZengeLife Sciences Publications LtdeLife2050-084X2017-01-01610.7554/eLife.18855Metabolite exchange between microbiome members produces compounds that influence Drosophila behaviorCaleb N Fischer0https://orcid.org/0000-0003-4223-8511Eric P Trautman1Jason M Crawford2https://orcid.org/0000-0002-7583-1242Eric V Stabb3Jo Handelsman4Nichole A Broderick5https://orcid.org/0000-0002-6830-9456Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United StatesDepartment of Chemistry, Yale University, New Haven, United StatesDepartment of Chemistry, Yale University, New Haven, United StatesDepartment of Microbiology, University of Georgia, Athens, United StatesDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United StatesDepartment 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 StatesAnimals 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.https://elifesciences.org/articles/18855microbiotahost-microbe interactionsolfactionmetabolismmicrobe-microbe interactions |
| spellingShingle | Caleb N Fischer Eric P Trautman Jason M Crawford Eric V Stabb Jo Handelsman Nichole A Broderick Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior eLife microbiota host-microbe interactions olfaction metabolism microbe-microbe interactions |
| 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 | microbiota host-microbe interactions olfaction metabolism microbe-microbe interactions |
| url | https://elifesciences.org/articles/18855 |
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