Microbiome potentiates endurance exercise through intestinal acetate production

The intestinal microbiome produces short-chain fatty acids (SCFAs) from dietary fiber and has specific effects on other organs. During endurance exercise, fatty acids, glucose, and amino acids are major energy substrates. However, little is known about the role of SCFAs during exercise. To investiga...

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Bibliographic Details
Published in:American journal of physiology: endocrinology and metabolism 2019-05, Vol.316 (5), p.E956-E966
Main Authors: Okamoto, Takuya, Morino, Katsutaro, Ugi, Satoshi, Nakagawa, Fumiyuki, Lemecha, Mengistu, Ida, Shogo, Ohashi, Natsuko, Sato, Daisuke, Fujita, Yukihiro, Maegawa, Hiroshi
Format: Article
Language:English
Subjects:
Accessibility
Acetates - metabolism
Acetic acid
Amino acids
Animals
Anti-Bacterial Agents - pharmacology
Antibiotics
Butyrates - metabolism
Carbohydrates
Cecum
Diet
Dietary fiber
Dietary Fiber - metabolism
Endurance capacity
Energy resources
Fatigue tests
Fatty acids
Fatty Acids, Volatile - metabolism
Fecal Microbiota Transplantation
Fecal microflora
Gastrointestinal Microbiome - drug effects
Gastrointestinal Microbiome - physiology
High carbohydrate diet
Intestine
Low carbohydrate diet
Metabolism
Mice
Microbiomes
Nutrient deficiency
Organs
Physical Conditioning, Animal
Physical Endurance - drug effects
Physical Endurance - physiology
Physical training
Propionates - metabolism
Propionic acid
Substrates
Transplantation
Treadmills
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Summary:The intestinal microbiome produces short-chain fatty acids (SCFAs) from dietary fiber and has specific effects on other organs. During endurance exercise, fatty acids, glucose, and amino acids are major energy substrates. However, little is known about the role of SCFAs during exercise. To investigate this, mice were administered either multiple antibiotics or a low microbiome-accessible carbohydrate (LMC) diet, before endurance testing on a treadmill. Two-week antibiotic treatment significantly reduced endurance capacity versus the untreated group. In the cecum acetate, propionate, and butyrate became almost undetectable in the antibiotic-treated group, plasma SCFA concentrations were lower, and the microbiome was disrupted. Similarly, 6-wk LMC treatment significantly reduced exercise capacity, and fecal and plasma SCFA concentrations. Continuous acetate but not saline infusion in antibiotic-treated mice restored their exercise capacity ( < 0.05), suggesting that plasma acetate may be an important energy substrate during endurance exercise. In addition, running time was significantly improved in LMC-fed mice by fecal microbiome transplantation from others fed a high microbiome-accessible carbohydrate diet and administered a single portion of fermentable fiber ( < 0.05). In conclusion, the microbiome can contribute to endurance exercise by producing SCFAs. Our findings provide new insight into the effects of the microbiome on systemic metabolism.
ISSN:0193-1849
1522-1555
DOI:10.1152/ajpendo.00510.2018