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 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.
Highlights
Multispecies microbial communities influence animal biology in diverse ways (McFallNgai et al, 2013): microbiomes modulate disease (van Nood et al, 2013), metabolize nutrients (Zhu et al, 2011), synthesize vitamins (Degnan et al, 2014), and modify behavior (Bravo et al, 2011)
To determine whether Drosophila responds to emergent microbial community metabolites, we used the T-maze olfactory assay to analyze Drosophila behavioral responses to several Drosophila microbiome members grown individually or in communities (Figure 1A, Supplementary file 2, Figure 1— figure supplement 1)
Focusing on a model Saccharomyces cerevisiae and Acetobacter malorum community, we found that when tested against apple juice medium (AJM), Drosophila attraction to the community was stronger than to the separate-culture mixture or individual members (Figure 1E)
Summary
Multispecies microbial communities (microbiomes) influence animal biology in diverse ways (McFallNgai et al, 2013): microbiomes modulate disease (van Nood et al, 2013), metabolize nutrients (Zhu et al, 2011), synthesize vitamins (Degnan et al, 2014), and modify behavior (Bravo et al, 2011). A central goal in host-microbiome studies is to understand the molecular mechanisms underpinning these diverse microbiome functions. Some aspects of microbial community function are the product of inter-species interactions (Rath and Dorrestein, 2012; Manor et al, 2014; Gerber, 2014; Gonzalez et al, 2012). Despite current understanding of microbial inter-species interactions in vitro, some of which has been elucidated in exquisite detail, the consequences of microbial
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