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

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 exer...

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Autores principales: Scheiman, Jonathan, Luber, Jacob M., Chavkin, Theodore A., MacDonald, Tara, Tung, Angela, Pham, Loc-Duyen, Wibowo, Marsha C., Wurth, Renee C., Punthambaker, Sukanya, Tierney, Braden T., Yang, Zhen, Hattab, Mohammad W., Avila-Pacheco, Julian, Clish, Clary B., Lessard, Sarah, Church, George M., Kostic, Aleksandar D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7368972/
https://www.ncbi.nlm.nih.gov/pubmed/31235964
http://dx.doi.org/10.1038/s41591-019-0485-4
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author Scheiman, Jonathan
Luber, Jacob M.
Chavkin, Theodore A.
MacDonald, Tara
Tung, Angela
Pham, Loc-Duyen
Wibowo, Marsha C.
Wurth, Renee C.
Punthambaker, Sukanya
Tierney, Braden T.
Yang, Zhen
Hattab, Mohammad W.
Avila-Pacheco, Julian
Clish, Clary B.
Lessard, Sarah
Church, George M.
Kostic, Aleksandar D.
author_facet Scheiman, Jonathan
Luber, Jacob M.
Chavkin, Theodore A.
MacDonald, Tara
Tung, Angela
Pham, Loc-Duyen
Wibowo, Marsha C.
Wurth, Renee C.
Punthambaker, Sukanya
Tierney, Braden T.
Yang, Zhen
Hattab, Mohammad W.
Avila-Pacheco, Julian
Clish, Clary B.
Lessard, Sarah
Church, George M.
Kostic, Aleksandar D.
author_sort Scheiman, Jonathan
collection PubMed
description 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 Veillonella relative abundance in marathon runners post-marathon and isolated a strain of Veillonella atypica from stool samples. Inoculation of this strain into mice significantly increased exhaustive treadmill runtime. Veillonella utilize lactate as their sole carbon source, which prompted us to perform 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 post-exercise. 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 runtime performance observed with V. atypica gavage. Taken together, these studies reveal that V. atypica improves runtime 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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spelling pubmed-73689722020-07-19 Meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism Scheiman, Jonathan Luber, Jacob M. Chavkin, Theodore A. MacDonald, Tara Tung, Angela Pham, Loc-Duyen Wibowo, Marsha C. Wurth, Renee C. Punthambaker, Sukanya Tierney, Braden T. Yang, Zhen Hattab, Mohammad W. Avila-Pacheco, Julian Clish, Clary B. Lessard, Sarah Church, George M. Kostic, Aleksandar D. Nat Med Article 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 Veillonella relative abundance in marathon runners post-marathon and isolated a strain of Veillonella atypica from stool samples. Inoculation of this strain into mice significantly increased exhaustive treadmill runtime. Veillonella utilize lactate as their sole carbon source, which prompted us to perform 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 post-exercise. 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 runtime performance observed with V. atypica gavage. Taken together, these studies reveal that V. atypica improves runtime via its metabolic conversion of exercise-induced lactate into propionate, thereby identifying a natural, microbiome-encoded enzymatic process that enhances athletic performance. 2019-06-24 2019-07 /pmc/articles/PMC7368972/ /pubmed/31235964 http://dx.doi.org/10.1038/s41591-019-0485-4 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Scheiman, Jonathan
Luber, Jacob M.
Chavkin, Theodore A.
MacDonald, Tara
Tung, Angela
Pham, Loc-Duyen
Wibowo, Marsha C.
Wurth, Renee C.
Punthambaker, Sukanya
Tierney, Braden T.
Yang, Zhen
Hattab, Mohammad W.
Avila-Pacheco, Julian
Clish, Clary B.
Lessard, Sarah
Church, George M.
Kostic, Aleksandar D.
Meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
title Meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
title_full Meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
title_fullStr Meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
title_full_unstemmed Meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
title_short Meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
title_sort meta’omic analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7368972/
https://www.ncbi.nlm.nih.gov/pubmed/31235964
http://dx.doi.org/10.1038/s41591-019-0485-4
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