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High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity.

ABSTRACT: Diet and exercise underpin the risk of obesity-related metabolic disease. Diet alters the gut microbiota, which contributes to aspects of metabolic disease during obesity. Repeated exercise provides metabolic benefits during obesity. We assessed whether exercise could oppose changes in the taxonomic and predicted metagenomic characteristics of the gut microbiota during diet-induced obesity. We hypothesized that high-intensity interval training (HIIT) would counteract high-fat diet (HFD)-induced changes in the microbiota without altering obesity in mice. Compared with chow-fed mice, an obesity-causing HFD decreased the Bacteroidetes-to-Firmicutes ratio and decreased the genetic capacity in the fecal microbiota for metabolic pathways such as the tricarboxylic acid (TCA) cycle. After HFD-induced obesity was established, a subset of mice were HIIT for 6 wk, which increased host aerobic capacity but did not alter body or adipose tissue mass. The effects of exercise training on the microbiota were gut segment dependent and more extensive in the distal gut. HIIT increased the alpha diversity and Bacteroidetes/Firmicutes ratio of the distal gut and fecal microbiota during diet-induced obesity. Exercise training increased the predicted genetic capacity related to the TCA cycle among other aspects of metabolism. Strikingly, the same microbial metabolism indexes that were increased by exercise were all decreased in HFD-fed vs. chow diet-fed mice. Therefore, exercise training directly opposed some of the obesity-related changes in gut microbiota, including lower metagenomic indexes of metabolism. Some host and microbial pathways appeared similarly affected by exercise. These exercise- and diet-induced microbiota interactions can be captured in feces.

SUBMITTER: Denou E

PROVIDER: S-EPMC4935139 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity.

Denou Emmanuel E Marcinko Katarina K Surette Michael G MG Steinberg Gregory R GR Schertzer Jonathan D JD

American journal of physiology. Endocrinology and metabolism 20160426 11

Diet and exercise underpin the risk of obesity-related metabolic disease. Diet alters the gut microbiota, which contributes to aspects of metabolic disease during obesity. Repeated exercise provides metabolic benefits during obesity. We assessed whether exercise could oppose changes in the taxonomic and predicted metagenomic characteristics of the gut microbiota during diet-induced obesity. We hypothesized that high-intensity interval training (HIIT) would counteract high-fat diet (HFD)-induced ...[more]

PMID: 27117007

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Project description:INTRODUCTION:Intestinal metabolism and microbiota profiles are impaired in obesity and insulin resistance. Moreover, dysbiotic gut microbiota has been suggested to promote systemic low-grade inflammation and insulin resistance through the release of endotoxins particularly lipopolysaccharides. We have previously shown that exercise training improves intestinal metabolism in healthy men. To understand whether changes in intestinal metabolism interact with gut microbiota and its release of inflammatory markers, we studied the effects of sprint interval (SIT) and moderate-intensity continuous training (MICT) on intestinal metabolism and microbiota in subjects with insulin resistance. METHODS:Twenty-six, sedentary subjects (prediabetic, n = 9; type 2 diabetes, n = 17; age, 49 [SD, 4] yr; body mass index, 30.5 [SD, 3]) were randomized into SIT or MICT. Intestinal insulin-stimulated glucose uptake (GU) and fatty acid uptake (FAU) from circulation were measured using positron emission tomography. Gut microbiota composition was analyzed by 16S rRNA gene sequencing and serum inflammatory markers with multiplex assays and enzyme-linked immunoassay kit. RESULTS:V?O2peak improved only after SIT (P = 0.01). Both training modes reduced systematic and intestinal inflammatory markers (tumor necrosis factor-?, lipopolysaccharide binding protein) (time P < 0.05). Training modified microbiota profile by increasing Bacteroidetes phylum (time P = 0.03) and decreasing Firmicutes/Bacteroidetes ratio (time P = 0.04). Moreover, there was a decrease in Clostridium genus (time P = 0.04) and Blautia (time P = 0.051). Only MICT decreased jejunal FAU (P = 0.02). Training had no significant effect on intestinal GU. Colonic GU associated positively with Bacteroidetes and inversely with Firmicutes phylum, ratio Firmicutes/Bacteroidetes and Blautia genus. CONCLUSIONS:Intestinal substrate uptake associates with gut microbiota composition and whole-body insulin sensitivity. Exercise training improves gut microbiota profiles and reduces endotoxemia.

Project description:PurposeObesity in children and in adolescents can lead to adult cardiovascular diseases, and the gut microbiota plays a crucial role in obesity pathophysiology. Exercise and diet interventions are typical approaches to improve physical condition and to alter the gut microbiota in individuals with obesity. However, whether central hemodynamic parameters including subendocardial viability ratio, the augmentation index standardized to a heart rate of 75/min (AIx75), resting heart rate, and blood pressure, correlate with gut microbiota changes associated with exercise and diet is unclear.MethodsAdolescents (n = 24, 12.88 ± 0.41 years) with obesity completed our 6-week program of endurance and strength exercises along with dietary restriction. Blood and fecal samples were collected, and physical parameters were measured before and 24 h after the last session of the intervention program. Pulse wave analysis using applanation tonometry provided the subendocardial viability ratio, a surrogate measure of microvascular myocardial perfusion, and AIx75, a measure of arterial stiffness and peripheral arteriolar resistance. Correlation analysis detected any associations of anthropometric or central hemodynamic parameters with gut microbiome composition.ResultsExercise and diet interventions significantly reduced body weight, body mass index, body fat, and waist-to-hip ratio, and lowered levels of fasting blood glucose, serum triglycerides, and high-density lipoprotein cholesterol. AIx75 and resting heart rate were also significantly reduced after the intervention without changes to systolic or diastolic blood pressure. The ratio of intestinal microbiota Firmicutes to Bacteroidetes displayed a marked increase after intervention. Interventional changes in gut microbiota members were significantly associated with anthropometric and metabolic parameters. Microbial changes were also significantly correlated with central hemodynamic parameters, including subendocardial viability ratio, AIx75, and resting heart rate.ConclusionExercise and diet interventions significantly improved measures of central hemodynamics, including subendocardial viability ratio, AIx75, and resting heart rate, which were correlated with altered gut microbiota in adolescents with obesity. Our findings shed light on the effects and mechanisms underlying exercise and diet interventions on obesity and suggest this approach for treating patients with both cardiovascular disease and obesity.

Dataset Information

High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity.

Publications

High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity.

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