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Nat Med. 2019 Jul;25(7):1104-1109. doi: 10.1038/s41591-019-0485-4. Epub 2019 Jun 24.

Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism.

Scheiman J1,2,3, Luber JM4,5,6,7,8, Chavkin TA4,5,7, MacDonald T9,10, Tung A1,2, Pham LD4,5, Wibowo MC4,5,7, Wurth RC3,11, Punthambaker S1,2, Tierney BT4,5,6,7, Yang Z4,5,12, Hattab MW2, Avila-Pacheco J8, Clish CB8, Lessard S9,10, Church GM13,14, Kostic AD15,16,17.

Author information

1
Department of Genetics, Harvard Medical School, Boston, MA, USA.
2
Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA, USA.
3
Fitbiomics, New York, NY, USA.
4
Section on Pathophysiology and Molecular Pharmacology, Joslin Diabetes Center, Boston, MA, USA.
5
Section on Islet Cell and Regenerative Biology, Joslin Diabetes Center, Boston, MA, USA.
6
Department of Biomedical Informatics, Harvard Medical School, Boston, MA, USA.
7
Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA, USA.
8
Broad Institute of MIT and Harvard, Cambridge, MA, USA.
9
Section on Clinical, Behavioral and Outcomes Research, Joslin Diabetes Center, Boston, MA, USA.
10
Department of Medicine, Harvard Medical School, Boston, MA, USA.
11
Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
12
Department of Combinatorics and Optimization, University of Waterloo, Waterloo, Ontario, Canada.
13
Department of Genetics, Harvard Medical School, Boston, MA, USA. gc@hms.harvard.edu.
14
Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA, USA. gc@hms.harvard.edu.
15
Section on Pathophysiology and Molecular Pharmacology, Joslin Diabetes Center, Boston, MA, USA. aleksandar.kostic@joslin.harvard.edu.
16
Section on Islet Cell and Regenerative Biology, Joslin Diabetes Center, Boston, MA, USA. aleksandar.kostic@joslin.harvard.edu.
17
Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA, USA. aleksandar.kostic@joslin.harvard.edu.

Abstract

The human gut microbiome is linked to many states of human health and disease1. 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 13C3-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.

PMID:
31235964
DOI:
10.1038/s41591-019-0485-4

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