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Hadza Prevotella require diet-derived microbiota-accessible carbohydrates to persist in mice.

ABSTRACT: 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.

SUBMITTER: Gellman RH

PROVIDER: S-EPMC10954246 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Hadza Prevotella require diet-derived microbiota-accessible carbohydrates to persist in mice.

Gellman Rebecca H RH Olm Matthew R MR Terrapon Nicolas N Enam Fatima F Higginbottom Steven K SK Sonnenburg Justin L JL Sonnenburg Erica D ED

Cell reports 20231028 11

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. Differ ...[more]

PMID: 38510311

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Project description:BackgroundWestern pattern diets induce neuroinflammation and impair cognitive behavior in humans and animals. Neuroinflammation and cognitive impairment have been associated with microbiota dysbiosis, through the gut-brain axis. Furthermore, microbiota-accessible carbohydrates (MACs) found in dietary fiber are important in shaping the microbial ecosystem and have the potential to improve the gut-brain-axis. However, the effects of MACs on neuroinflammation and cognition in an obese condition have not yet been investigated. The present study aimed to evaluate the effect of MACs on the microbiota-gut-brain axis and cognitive function in obese mice induced by a high-fat and fiber deficient (HF-FD) diet.MethodsC57Bl/6 J male mice were fed with either a control HF-FD or a HF-MAC diet for 15 weeks. Moreover, an additional group was fed with the HF-MAC diet in combination with an antibiotic cocktail (HF-MAC + AB). Following the 15-week treatment, cognitive behavior was investigated; blood, cecum content, colon, and brain samples were collected to determine metabolic parameters, endotoxin, gut microbiota, colon, and brain pathology.ResultsWe report MACs supplementation prevented HF-FD-induced cognitive impairment in nesting building and temporal order memory tests. MACs prevented gut microbiota dysbiosis, including increasing richness, α-diversity and composition shift, especially in Bacteroidetes and its lower taxa. Furthermore, MACs increased colonic mucus thickness, tight junction protein expression, reduced endotoxemia, and decreased colonic and systemic inflammation. In the hippocampus, MACs suppressed HF-FD-induced neuroglia activation and inflammation, improved insulin IRS-pAKT-pGSK3β-pTau synapse signaling, in addition to the synaptic ultrastructure and associated proteins. Furthermore, MACs' effects on improving colon-cognitive parameters were eliminated by wide spectrum antibiotic microbiota ablation.ConclusionsThese results suggest that MACs improve cognitive impairments via the gut microbiota-brain axis induced by the consumption of an HF-FD. Supplemental MACs to combat obesity-related gut and brain dysfunction offer a promising approach to prevent neurodegenerative diseases associated with Westernized dietary patterns and obesity.

Project description:Whole grains are generally low in nondigestible carbohydrates that are available for fermentation by the gut microbiota, or microbiota-accessible carbohydrates (MAC). However, there is potential to increase MAC in whole grains through food processing. Five processing methods: boiling, extrusion, sourdough bread, unleavened bread, and yeast bread, were applied to whole wheat flour and then subjected to in vitro digestion followed by fermentation using fecal microbiomes from 10 subjects. The microbiomes separated into 2 groups: those that showed high carbohydrate utilization (CU) and those that exhibited low CU. The former exhibited not only enhanced CU but also increased butyrate production (MAC, 31.1 ± 1.1% versus 19.3 ± 1.2%, P < 0.001; butyrate, 5.26 ± 0.26 mM versus 3.17 ± 0.27 mM, P < 0.001). Only the microbiomes in the high-CU group showed significant differences among processing methods: extrusion and sourdough bread led to dichotomous results for MAC and short-chain fatty acid production, where extrusion resulted in high MAC but low butyrate production while sourdough bread resulted in low MAC but high butyrate production. Extrusion led to a noticeable decrease in α-diversity and some members of the families Ruminococcaceae and Lachnospiraceae, with increases in Acinetobacter, Enterococcus, and Staphylococcaceae This study demonstrated that only microbiomes that exhibited high CU responded to the effects of processing by showing significant differences among processing methods. In these microbiomes, extrusion was able to increase accessibility of the cell wall polysaccharides but did not increase butyrate production. In contrast, sourdough bread led to high butyrate production by supporting important butyrate-producers in the families Lachnospiraceae and RuminococcaceaeIMPORTANCE Dietary nondigestible carbohydrates, or dietary fiber, have long been recognized for their beneficial health effects. However, recent studies have revealed that fermentation of nondigestible carbohydrates by gut bacteria is critical in mediating many of the health-promoting properties of dietary fibers. Whole grains are excellent candidates to supply the microbiome with a plentiful source of nondigestible carbohydrates, although unfortunately a majority of these carbohydrates in whole grains are not available to gut bacteria for fermentation. Processing is known to alter the structural characteristics of nondigestible carbohydrates in whole grains, yet the relationship between these effects and gut microbial fermentation is unknown. This research aimed to address this important research gap by identifying interactions between whole-grain processing and gut bacteria, with the ultimate goal of increasing the availability of nondigestible carbohydrates for fermentation to enhance host health.

Project description:While the gut microbiota is known to be influenced by habitual food intake, this relationship is seldom explored in type 2 diabetes patients. This study aims to investigate the relationship between dietary patterns and gut microbial species abundance in 113 type 2 diabetes patients (mean age, 58 years; body mass index, 29.1; glycohemoglobin [HbA1c], 8.1%). We analyzed the gut microbiota using 16S amplicon sequencing, and all patients were categorized into either the Bacteroides enterotype (57.5%, n = 65) or the Prevotella enterotype (42.5%, n = 48) using the partitioning around medoids clustering algorithm, based on the most representative genera. Patients with the Bacteroides enterotype showed better glycemic control with a 2.71 odds of HbA1c ≤ 7.0% compared to the Prevotella enterotype (95% confidence interval, 1.02-7.87; P, 0.034). Dietary habits and the nutrient composition of all patients were assessed using a validated food frequency questionnaire. It was observed that the amounts of dietary fiber consumed were suboptimal, with an average intake of 16 g per day. Additionally, we extracted four dietary patterns through factor analysis: eating-out, high-sugar foods, fish-vegetable, and fermented foods patterns. Patients with the Bacteroides enterotype had higher scores for the fish-vegetable pattern compared to the Prevotella enterotype (0.17 ± 0.13 versus -0.23 ± 0.09; P, 0.010). We further investigated the relationship between the microbiota and the four dietary patterns and found that only the fish-vegetable dietary pattern scores were correlated with principal coordinate values. A lower pattern score was associated with the accumulated abundance of the 31 significant microbial features. Among these features, Prevotella copri was identified as the most significant by using a random forest model, with an area under the receiver operating characteristic of 0.93 (95% confidence interval, 0.88-0.98). To validate these results, we conducted a custom quantitative polymerase chain reaction assay. This assay confirmed the presence of P. copri (sensitivity, 0.96; specificity, 0.97) in our cohort, with a prevalence of 47.8%, and a mean relative abundance of 21.0% in subjects harboring P. copri. In summary, type 2 diabetes patients with the Prevotella enterotype demonstrated poorer glycemic control and deviations from a healthy dietary pattern. The abundance of P. copri, as a major contributing microbial feature, was associated with the severity in the deficiency in dietary fish and vegetables. Emphasis should be placed on promoting a healthy dietary pattern and understanding the microbial correlations.

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Hadza Prevotella require diet-derived microbiota-accessible carbohydrates to persist in mice.

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Hadza <i>Prevotella</i> require diet-derived microbiota-accessible carbohydrates to persist in mice.

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