Nutrients from the host diet and microbial cross-feeding allow diverse bacteria to colonize the animal gut. Less is known about the role of host-derived nutrients in enabling gut bacterial colonization. We examined metabolic interactions within the evolutionary ancient symbiosis between the honey bee (Apis mellifera) and the core gut microbiota memberSnodgrassella alvi. This Betaproteobacteria is incapable of metabolizing saccharides, yet colonizes the honey bee gut in the presence of only a sugar diet. Using comparative metabolomics,13C tracers, and Nanoscale secondary ion mass spectrometry (NanoSIMS), we showin vivothatS. alvigrows on host-derived organic acids, including citrate, glycerate and 3-hydroxy-3-methylglutarate which are actively secreted by the host into the gut lumen.S. alviadditionally modulates tryptophan metabolism in the gut, primarily by converting kynurenine to anthranilate. These results suggest thatSnodgrassellais adapted to a specific metabolic niche in the gut that depends on host-derived nutritional resources.

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