Bacteroides uniformis enhances endurance exercise performance through gluconeogenesis

Abstract

Athletes require high levels of energy to exercise under extreme conditions. Gut microbiota supplies energy to the host; however, the mechanism how gut microbiota contribute in the athlete is unclear. In this study, we determined that gut microbiota of Japanese long-distance runners differed from that of non-athletes, and the Bacteroides uniformis cell number in the feces correlated with 3,000-m race time. Mice administrated with B. uniformis extended the swimming time to exhaustion. Furthermore, acetate and propionate concentrations in the cecum increased in B. uniformis-administered mice subjected to weekly exercise.Expression levels of carnitine palmitoyl transferase 1a and phosphoenolpyruvate carboxykinase genes were elevated in the liver, suggesting that acetate and propionate produced by B. uniformis improve endurance exercise performance, at least in part, through enhancing gluconeogenesis. In addition, α-cyclodextrin administration increased B. uniformis and improved the performance in humans and mice, thus it is a candidate substance enhancing exercise performance through modification of gut microbiota. INTRODUCTIONHuman exercise performance comprises a combination of physical strength (e.g., muscle and explosive strength, endurance, and flexibility) and the actions performed in a given exercise (e.g., throwing, kicking, and hitting). Exercise performance can be improved through training; however, other factors, such as genetic background, may affect it. Recently, several reports have demonstrated that the gut microbiota contributes to health, energy homeostasis, and glucose and lipid metabolisms 1-4 . Hsu et al. reported that the swimming endurance time of germ-free mice was shorter than that of specific-pathogen-free mice and Bacteroides fragilis-monoassociated mice, thus identifying gut microbiota as one of the factors associated with exercise performance 5 . Conversely, other studies have shown that exercise changes the gut microbiome profile in mice 6,7 . In humans, Clarke et al. reported that the gut microbiota of rugby players had high α diversity and relative abundance of the genera Prevotella, Succinivibrio, Bacteroides, and Lactobacillus, as a difference to those of non-rugby players 8 . Another study on the gut microbiota of cyclists showed that a high abundance ofPrevotella was correlated with weekly exercise time 9 . However, none of these studies demonstrated a causal relationship between exercise performance and characteristic genera in the gut microbiota of athletes. Recently, Veillonella atypica, isolated from the gut microbiota of marathon runners, was shown to produce propionate from exercise-induced lactate in the gut, improving endurance exercise performance in mice 10 . Only that report has demonstrated a causal relationship between exercise performances and the gut microbiota in mice, but 3 detailed relationship remains unclear. In the present study, we investigated the role of Bacteroides uniformis, identified in the microbiome analysis of Japanese long-distance runners, in the en...

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