Industrialization has transformed the gut microbiota, reducing the prevalence of Prevotellarelative to Bacteroides. Here, we isolate Bacteroidesand Prevotellastrains from the microbiota of Hadza hunter-gatherers of Tanzania, a population with high levels of Prevotella. We demonstrate that plant-derived microbiota-accessible carbohydrates (MACs) are required for persistence of Prevotella copribut not Bacteroides thetaiotaomicron in vivo. Differences in carbohydrate metabolism gene content, expression, and in vitrogrowth reveal that Hadza Prevotellastrains specialize in degrading plant carbohydrates, while Hadza Bacteroidesisolates use both plant and host-derived carbohydrates, a difference mirrored in Bacteroidesfrom non-Hadza populations. When competing directly, P. coprirequires plant-derived MACs to maintain colonization in the presence of B. thetaiotaomicron,as a no MAC diet eliminates P. copricolonization. Prevotella’sreliance on plant-derived MACs and Bacteroides’ability to use host mucus carbohydrates could explain the reduced prevalence of Prevotellain populations consuming a low-MAC, industrialized diet.