Energy status alters intestinal function and the gut microbiota during consecutive days of high energy demands

Host-gut microbiota interactions may impact intestinal function during sustained periods of high energy demands. Whether energy status, reflecting the balance between energy intake and expenditure, impacts those interactions is unknown. This study determined the effects of energy status during sustained high-energy demands on intestinal function and the gut microbiota. Ten healthy men completed a randomized, crossover study that included baseline (BL) testing and two 72-hour periods of high physical activity-induced energy demands (HPA; ∼2,300 kcal/day physical activity energy expenditure) followed by a 7-day recovery period (REC). During HPA, diets designed to elicit a ∼45% energy deficit (DEF; -2,047 ± 920 kcal/day) or maintain energy balance within ±10% total daily energy expenditure (BAL; 689 ± 852 kcal/day) were provided. Intestinal permeability and transit time, fecal microbiota composition and gene content, fecal short-chain fatty acids (SCFAs), and gastrointestinal symptoms were measured. Intestinal permeability was 17% higher during HPA-DEF vs. HPA-BAL (P = 0.02), and colonic transit time was slower during HPA-DEF vs. HPA-BAL [mean difference (95% CI) = -764 min (-1,345, -183)] and BL [-643 min (-1,178, -108)] (P ≤ 0.02). Fecal microbiota species richness [-40 species (-66, -13), P = 0.01] and relative abundances of multiple species (log₂ fold difference < -5, P < 0.02) were lower during HPA-BAL vs. HPA-DEF but did not differ between conditions during REC. Small bowel transit time, gastrointestinal symptoms, fecal microbiota gene pathways, and fecal SCFAs did not differ between conditions. Findings suggest that increasing dietary intake to prevent energy deficit may benefit intestinal health and function during short-term periods of high energy demands without sustained impacts on the gut microbiota.NEW & NOTEWORTHY The effect of energy status on host-gut microbiota interactions impacting intestinal function during periods of high energy demands is unknown. Herein, increasing energy intake to prevent energy deficit during three days of high physical activity-induced energy demands prevented increases in intestinal permeability and transit time, and transiently reduced gut microbiota community richness without compromising community functional potential. Results suggest minimizing energy deficits may benefit gastrointestinal function during periods of high energy demands.