Aerobic exercise training‐induced alteration of gut microbiota composition affects endurance capacity

• Published in: The Journal of physiology Vol. 601; no. 12; pp. 2329 - 2344
• Main Authors: Uchida, Masataka, Fujie, Shumpei, Yano, Hiromi, Iemitsu, Motoyuki
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.06.2023
• Subjects: Aerobic capacity; Aerobics; Alcaligenaceae; Animals; Anti-Bacterial Agents; Antibiotics; Citrate (si)-Synthase - metabolism; Citrate synthase; Digestive system; endurance performance; Energy metabolism; Erysipelotrichaceae; Exercise; exercise training; Fitness equipment; Fitness training programs; Gastrocnemius muscle; Gastrointestinal Microbiome; gut microbiome; Intestinal microflora; Metabolism; Mice; Mice, Inbred ICR; Microbiota; Muscle, Skeletal - physiology; Musculoskeletal system; Physical Conditioning, Animal - physiology; Physical Endurance - physiology; Physical fitness; Physical training; Running; Skeletal muscle; trainability; Transplantation; endurance performance; gut microbiome; trainability; exercise training
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/JP283995

This study aimed to clarify whether aerobic exercise training‐induced alterations in the gut microbiota affect physiological adaptation with endurance exercise capacity. In study 1, ICR mice were randomly divided into three groups: vehicle intake + sedentary (V+S), vehicle intake + exercise training (V+Ex) and antibiotic intake + exercise training (AB+Ex). In the exercise training groups, treadmill running was performed for 8 weeks. During the exercise training intervention, the antibiotic‐intake group freely drank water containing antibiotics. In study 2, ICR mice were randomly divided into three groups: Sham, transplantation of caecum microbiota from sedentary mice (Sed‐CMT) and exercise training mice (Ex‐CMT). In study 1, the treadmill running time to exhaustion, an index of maximal aerobic capacity, after aerobic exercise training in the V+Ex group was significantly longer than that in the V+S and AB+Ex groups. Gastrocnemius muscle citrate synthase (CS) activity and PGC‐1α protein levels in the V+Ex group were significantly higher than in the V+S and AB+Ex groups. The bacterial Erysipelotrichaceae and Alcaligenaceae families were positively correlated with treadmill running time to exhaustion. In study 2, the treadmill running time to exhaustion after transplantation was significantly higher in the Ex‐CMT group than in the Sham and Sed‐CMT groups. Furthermore, CS activity and PGC‐1α protein levels in the gastrocnemius muscle were significantly higher in the Ex‐CMT group than in the Sham and Sed‐CMT groups. Thus, gut microbiota altered by aerobic exercise training may be involved in the augmentation of endurance capacity and muscle mitochondrial energy metabolism. Key points Aerobic exercise training changes gut microbiota composition, and the Erysipelotrichaceae and Alcaligenaceae families were among the altered gut bacteria. The gut microbiota was associated with endurance performance and metabolic regulator levels in skeletal muscle after aerobic exercise training. Continuous antibiotic treatment attenuated the increase in endurance performance, citrate synthase activity and PGC‐1α levels in skeletal muscle induced by aerobic exercise training. Gut microbiota transplantation from exercise‐trained mice improved endurance performance and metabolic regulator levels in recipient skeletal muscle, despite the absence of aerobic exercise training. figure legend Study 1: in mice with or without the antibiotic treatment, aerobic treadmill running was performed for 8 weeks. In the trained mice with vehicle treatment, aerobic exercise training changed gut microbiota composition and induced augmentation of running time, muscle citrate synthase (CS) activity and PGC‐1α levels, but continuous antibiotic treatment attenuated the training effects. Study 2: mice were transplanted with caecum microbiota of exercise‐trained mice. The transplanted mice showed augmentation of running time, muscle CS activity and PGC‐1α levels. These findings suggest that gut microbiota altered by aerobic exercise training may be involved in the augmentation of endurance capacity and muscle mitochondrial energy metabolism.