Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
Open accessAbstract
The human gut microbiome is linked to many states of human health and disease 1. The metabolic repertoire of the gut microbiome is vast, but the health implications of these bacterial pathways are poorly understood. In this study, we identify a link between members of the genus Veillonella and exercise performance. We observed an increase in Veillonella relative abundance in marathon runners postmarathon and isolated a strain of Veillonella atypica from stool samples. Inoculation of this strain into mice significantly increased exhaustive treadmill run time. Veillonella utilize lactate as their sole carbon source, which prompted us to perform a shotgun metagenomic analysis in a cohort of elite athletes, finding that every gene in a major pathway metabolizing lactate to propionate is at higher relative abundance postexercise. Using 13 C 3-labeled lactate in mice, we demonstrate that serum lactate crosses the epithelial barrier into the lumen of the gut. We also show that intrarectal instillation of propionate is sufficient to reproduce the increased treadmill run time performance observed with V. atypica gavage. Taken together, these studies reveal that V. atypica improves run time via its metabolic conversion of exercise-induced lactate into propionate, thereby identifying a natural, microbiome-encoded enzymatic process that enhances athletic performance.
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The microbiota has an indirect influence on various indices of exercise performance, recovery, and patterns of illness, such as signaling through myokines and other cytokines, modulating activation of the hypothalamic-pituitary-adrenal axis, and affecting performance-associated metabolic pathways.
“The microbiota has an indirect influence on various indices of exercise performance, recovery, and patterns of illness, such as signaling through myokines and other cytokines, modulating activation of the hypothalamic–pituitary–adrenal axis, and affecting performance-associated metabolic pathways [13, 16–18].”
From The athletic gut microbiota (2020) · cites this paper as [16]
Veillonella was more prevalent among runners compared to non-runners.
“Additionally, Veillonella was more prevalent among runners compared to non-runners.”
From The athletic gut microbiota (2020) · cites this paper as [16]
The relative abundance of Veillonella increased after the marathon and was the most differentially abundant microbial feature between pre- and post-exercise states.
“The relative abundance of the bacterial genus Veillonella increased after the marathon and was the most differentially abundant microbial feature between the pre- and post-exercise states.”
From The athletic gut microbiota (2020) · cites this paper as [16]
In a preclinical crossover trial, Veillonella-inoculated mice had a 13% improvement in time to exhaustion running tests and significant reductions in inflammatory cytokines post exercise compared to control.
“In a pre-clinical crossover trial, Veillonella inoculated mice had a 13% improvement in time to exhaustion running tests as well as significant reductions in inflammatory cytokines post exercise compared to control.”
From The athletic gut microbiota (2020) · cites this paper as [16]
Veillonella-inoculated mice more effectively converted lactate to the SCFA propionate.
“They also more effectively converted lactate to the SCFAs propionate.”
From The athletic gut microbiota (2020) · cites this paper as [16]
In a second experiment, relative taxonomic abundances of Veillonella increased post-exercise.
“Similar findings were reproduced as relative taxonomic abundances Veillonella were increased post-exercise.”
From The athletic gut microbiota (2020) · cites this paper as [16]
Systemic lactate in these animals was able to cross the gut barrier into the lumen, making it available as a substrate for microbial SCFA conversion.
“Importantly, Scheiman et al. [16] found systemic lactate in these animals was able to cross the gut barrier into the lumen, making it available as a substrate for microbial SCFA conversion.”
From The athletic gut microbiota (2020) · cites this paper as [16]
The Veillonella methylmalonyl-CoA pathway was overrepresented in metagenomic samples post-exercise across the cohort.
“In addition, the Veillonella methylmalonyl-CoA pathway was overrepresented in the metagenomic samples post-exercise across the cohort.”
From The athletic gut microbiota (2020) · cites this paper as [16]
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Background
- Authors
- Scheiman, J., Luber, J. M., Chavkin, T. A., MacDonald, T., Tung, A., Pham, L.-D., Wibowo, M. C., Wurth, R. C., Punthambaker, S., Tierney, B. T., Yang, Z., Hattab, M. W., Avila-Pacheco, J., Clish, C. B., Lessard, S., Church, G. M., & Kostic, A. D.
- Affiliations
- Harvard University (US)
- Broad Institute (US)
- Joslin Diabetes Center (US)
- Corresponding author
- Church, George M.
- Kostic, Aleksandar D.
- ORCID
- Venue
- Nature Medicine
- Published
- 2019-06-24
- Volume
- 25
- Issue
- 7
- Pages
- 1104-1109
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC7368972
- OpenAlex
- W2949339202
- Cited by
- 892
- References
- 34
- Citations by year
- 2026: 131 · 2025: 132 · 2024: 139 · 2023: 134 · 2022: 115 · 2021: 108 · 2020: 102 · 2019: 29
- FWCI
- 29.30
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Human Genome Research Institute (T32HG002295)
- National Institute of Diabetes and Digestive and Kidney Diseases (T32DK007260, P30DK036836, P30DK040561)
- U.S. National Library of Medicine (T15LM007092)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- gut microbiota, Veillonella atypica, lactate metabolism, propionate, athletic performance, marathon runners, exercise-induced lactate, serum lactate, endurance running
- MeSH terms
- Gastrointestinal Microbiome, Animals, Humans, Mice, Inbred C57BL, Propionates, Running, Veillonella, Exercise, Lactic Acid, Mice, Metagenomics, Athletes
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