Sugar ABC transporter repertoires predict ecological dynamics in gut microbiome communities

The gut microbiome plays a central role in human health, but modern diets and lifestyles alter its composition. Increased sugar consumption is a hallmark of modern diets, yet its impact on the microbiome remains poorly understood. Here, we combine comparative genomics, experiments, and longitudinal human diet-microbiome records to show that the response of the microbiome to dietary sugars is explained by the carriage of sugar ABC (ATP-binding cassette) transporters. Bacteria encoding these transporters exhibit enhanced growth and consistently outcompete others in both monocultures and complex consortia across contexts. Targeted deletion of sugar transporter genes in Escherichia coli, a model gut pathobiont of the expanded Oligo-Mouse-Microbiota (OMM15) consortium, reveals that a specific sugar ABC transporter gene is required to compete, and invade this community. In gnotobiotic mice colonized with the OMM15 consortium, dietary sugar supplementation selectively increases the expansion of sugar ABC transporter-positive bacteria, including E. coli. Paired human diet-microbiome data reveal that intake of dietary sugars significantly correlates with the expansion of sugar ABC transporter-positive genera. Taken together, our work identifies a genomic predictor of microbiome responses to dietary sugars and suggests ways to anticipate major shifts in the abundances of important gut bacteria.