Ultra-Endurance triathlon competition shifts fecal metabolome independent of changes to microbiome composition

Abstract

Understanding changes to gut microbiota composition and metabolic output in response to acute exercise may be necessary for understanding the mechanisms mediating the long-term health and performance benefits of exercise. Our primary objective was to characterize acute changes in the fecal microbiome and metabolome following participation in an ultra-endurance (3.9km swim, 180.2km bike, 42.2km run) triathlon. An exploratory aim was to determine associations between athlete-specific factors (race performance [i.e., completion time] and lifetime years of endurance training) with pre-race gut microbiota and metabolite profiles. Stool samples from 12 triathletes (9M/3F; 43±14 yrs, 23±2 kg/m2) were collected ≤48 hours before and the first bowel movement following race completion. Intra- and inter-individual diversity of bacterial species and individual bacterial taxa were unaltered following race completion (P>0.05). However, significant reductions (P<0.05) in free and secondary bile acids (DCA, 12-ketoLCA) and short-chain fatty acids (butyric and pivalic acids), and significant increases (P<0.05) in long-chain fatty acids (oleic and palmitoleic acids) were observed. Exploratory analyses revealed several associations between pre-race bacterial taxa and fecal metabolites with race performance and lifetime history of endurance training (P<0.05). These findings suggest that 1) acute ultra-endurance exercise shifts microbial metabolism independent of changes to community composition and 2) athlete performance level and training history relate to resting-state gut microbial ecology.

Gut check: Unveiling the influence of acute exercise on the gut microbiota

“…We identified nine studies that evaluated α‐diversity of the gut microbiota before and after an acute exercise bout in human participants. Five of the nine studies reported no differences (Grosicki, Pugh, et al., 2023 ; Oliveira et al., 2022 ; Sato & Suzuki, 2022 ; Tabone et al., 2021 ; Zhao et al., 2018 ), which is consistent with observations from 6‐ to 8‐week training studies in humans (Allen et al., 2018 ; Cronin et al., 2018 ) and mice (Lamoureux et al., 2017 ) reporting no changes in α‐diversity. However, cross‐sectional investigations report greater α‐diversity in athletes and physically active individuals compared with sedentary controls (Clarke et al., 2014 ).…”

“…Two investigations of acute exercise on microbiota responses (Grosicki, Pugh, et al., 2023 ; Oliveira et al., 2022 ), including our own (Grosicki, Pugh, et al., 2023 ), demonstrated no change in any bacterial species post‐exercise. While in contrast to many studies in this area, stability and resilience have been identified as essential ecological characteristics of the gut microbiota with relevance for human health (Fassarella et al., 2021 ).…”

“…β‐Diversity is determined by statistical techniques that quantify the distance between microbiota pairs, which can be evaluated using distance‐based hypothesis testing (e.g., permutational multivariate analysis of variance) (Kelly et al., 2015 ). Of the 11 studies that investigated the effects of acute exercise on the gut microbiota, only six included β‐diversity analyses, four of which reported no changes (Grosicki, Pugh, et al., 2023 ; Oliveira et al., 2022 ; Sato & Suzuki, 2022 ; Tabone et al., 2021 ) and two reported changes (Fukuchi et al., 2022 ; Karl et al., 2017 ). In our view, no immediate, distinguishable differences between these studies is apparent.…”

“…While diversity analyses reflect overall patterns in microbiota variation, a limitation of these techniques is that they may miss subtle changes in low‐abundance microbiota that may play important roles in host physiology (Su, 2021 ). To capture these changes, investigations have performed pairwise comparisons of amplicon sequence variants (ASVs), ranging from the phylum (Shukla et al., 2015 ) to the species level (Grosicki, Pugh, et al., 2023 ; Oliveira et al., 2022 ; Sato & Suzuki, 2022 ; Scheiman et al., 2019 ; Tabone et al., 2021 ). Of the 11 studies included in this review, nine reported changes in specific microbial taxa (Fukuchi et al., 2022 ; Grosicki et al., 2019 ; Karl et al., 2017 ; Keohane et al., 2019 ; Sato & Suzuki, 2022 ; Scheiman et al., 2019 ; Shukla et al., 2015 ; Tabone et al., 2021 ; Zhao et al., 2018 ).…”

“…Inspection of possible explanations for these inter‐study differences reveals a key limitation in the existing acute exercise microbiota literature. Specifically, only 2 of 11 studies, including our recent work demonstrating no changes in any bacterial species following an Ironman triathlon (Grosicki, Pugh, et al., 2023 ), implemented whole genome shotgun sequencing. Importantly, whole genome shotgun sequencing has multiple advantages over the 16S amplicon method including enhanced resolution and accurate identification of bacterial species as well as increased detection of diversity and prediction of genes (Ranjan et al., 2016 ).…”