Hadza Prevotella require diet-derived microbiota-accessible carbohydrates to persist in mice
Rebecca H. Gellman,
Matthew R. Olm,
Nicolas Terrapon,
Fatima Enam,
Steven K. Higginbottom,
Justin L. Sonnenburg,
Erica D. Sonnenburg
Affiliations
Rebecca H. Gellman
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA
Matthew R. Olm
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA
Nicolas Terrapon
Architecture et Fonction des Macromolécules Biologiques, INRAE, CNRS, Aix-Marseille Université, Marseille, France
Fatima Enam
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA
Steven K. Higginbottom
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA
Justin L. Sonnenburg
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA; Chan Zuckerberg Biohub, San Francisco, CA, USA; Center for Human Microbiome Studies, Stanford University School of Medicine, Stanford, CA, USA; Corresponding author
Erica D. Sonnenburg
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA; Center for Human Microbiome Studies, Stanford University School of Medicine, Stanford, CA, USA; Corresponding author
Summary: Industrialization has transformed the gut microbiota, reducing the prevalence of Prevotella relative to Bacteroides. Here, we isolate Bacteroides and Prevotella strains from the microbiota of Hadza hunter-gatherers in Tanzania, a population with high levels of Prevotella. We demonstrate that plant-derived microbiota-accessible carbohydrates (MACs) are required for persistence of Prevotella copri but not Bacteroides thetaiotaomicron in vivo. Differences in carbohydrate metabolism gene content, expression, and in vitro growth reveal that Hadza Prevotella strains specialize in degrading plant carbohydrates, while Hadza Bacteroides isolates use both plant and host-derived carbohydrates, a difference mirrored in Bacteroides from non-Hadza populations. When competing directly, P. copri requires plant-derived MACs to maintain colonization in the presence of B. thetaiotaomicron, as a no-MAC diet eliminates P. copri colonization. Prevotella’s reliance on plant-derived MACs and Bacteroides’ ability to use host mucus carbohydrates could explain the reduced prevalence of Prevotella in populations consuming a low-MAC, industrialized diet.