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The impact of commensal bacteria on the host arises from complex microbial-diet-host interactions. Mapping metabolic interactions in gut microbial communities is therefore key to understand how the microbiome influences the host. Here we use an interdisciplinary approach including isotope-resolved metabolomics to show that in  Drosophila melanogaster, Acetobacter pomorum  ( Ap ) and  Lactobacillus plantarum  ( Lp ) a syntrophic relationship is established to overcome detrimental host diets and identify  Ap  as the bacterium altering the host’s feeding decisions. Specifically, we show that  Ap  uses the lactate produced by  Lp  to supply amino acids that are essential to  Lp , allowing it to grow in imbalanced diets. Lactate is also necessary and sufficient for  Ap  to alter the fly’s protein appetite. Our data show that gut bacterial communities use metabolic interactions to become resilient to detrimental host diets. These interactions also ensure the constant flow of metabolites used by the microbiome to alter reproduction and host behaviour.

Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour