Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics

Abstract Recently, the gut microbiome has emerged as a potent modulator of exercise‐induced systemic adaptation and appears to be crucial for mediating some of the benefits of exercise. This study builds upon previous evidence establishing a gut microbiome‐skeletal muscle axis, identifying exercise‐...

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Main Authors: Ahmed Ismaeel, Taylor R. Valentino, Benjamin Burke, Jensen Goh, Tolulope P. Saliu, Fatmah Albathi, Allison Owen, John J. McCarthy, Yuan Wen
Format: Article
Language:English
Published: Wiley 2023-11-01
Series:Physiological Reports
Subjects:
Online Access:https://doi.org/10.14814/phy2.15848
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author Ahmed Ismaeel
Taylor R. Valentino
Benjamin Burke
Jensen Goh
Tolulope P. Saliu
Fatmah Albathi
Allison Owen
John J. McCarthy
Yuan Wen
author_facet Ahmed Ismaeel
Taylor R. Valentino
Benjamin Burke
Jensen Goh
Tolulope P. Saliu
Fatmah Albathi
Allison Owen
John J. McCarthy
Yuan Wen
author_sort Ahmed Ismaeel
collection DOAJ
description Abstract Recently, the gut microbiome has emerged as a potent modulator of exercise‐induced systemic adaptation and appears to be crucial for mediating some of the benefits of exercise. This study builds upon previous evidence establishing a gut microbiome‐skeletal muscle axis, identifying exercise‐induced changes in microbiome composition. Metagenomics sequencing of fecal samples from non‐exercise‐trained controls or exercise‐trained mice was conducted. Biodiversity indices indicated exercise training did not change alpha diversity. However, there were notable differences in beta‐diversity between trained and untrained microbiomes. Exercise significantly increased the level of the bacterial species Muribaculaceae bacterium DSM 103720. Computation simulation of bacterial growth was used to predict metabolites that accumulate under in silico culture of exercise‐responsive bacteria. We identified acetate and succinate as potential gut microbial metabolites that are produced by Muribaculaceae bacterium, which were then administered to mice during a period of mechanical overload‐induced muscle hypertrophy. Although no differences were observed for the overall muscle growth response to succinate or acetate administration during the first 5 days of mechanical overload‐induced hypertrophy, acetate and succinate increased skeletal muscle mitochondrial respiration. When given as post‐biotics, succinate or acetate treatment may improve oxidative metabolism during muscle hypertrophy.
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spelling doaj.art-eaa76897c15747e79d797f4010157bc22023-12-13T03:41:18ZengWileyPhysiological Reports2051-817X2023-11-011121n/an/a10.14814/phy2.15848Acetate and succinate benefit host muscle energetics as exercise‐associated post‐bioticsAhmed Ismaeel0Taylor R. Valentino1Benjamin Burke2Jensen Goh3Tolulope P. Saliu4Fatmah Albathi5Allison Owen6John J. McCarthy7Yuan Wen8Department of Physiology, College of Medicine University of Kentucky Lexington Kentucky USABuck Institute for Research on Aging Novato California USADepartment of Physiology, College of Medicine University of Kentucky Lexington Kentucky USADepartment of Physiology, College of Medicine University of Kentucky Lexington Kentucky USADepartment of Physiology, College of Medicine University of Kentucky Lexington Kentucky USADepartment of Pharmacology and Nutritional Sciences, College of Medicine University of Kentucky Lexington Kentucky USACenter for Muscle Biology University of Kentucky Lexington Kentucky USADepartment of Physiology, College of Medicine University of Kentucky Lexington Kentucky USADepartment of Physiology, College of Medicine University of Kentucky Lexington Kentucky USAAbstract Recently, the gut microbiome has emerged as a potent modulator of exercise‐induced systemic adaptation and appears to be crucial for mediating some of the benefits of exercise. This study builds upon previous evidence establishing a gut microbiome‐skeletal muscle axis, identifying exercise‐induced changes in microbiome composition. Metagenomics sequencing of fecal samples from non‐exercise‐trained controls or exercise‐trained mice was conducted. Biodiversity indices indicated exercise training did not change alpha diversity. However, there were notable differences in beta‐diversity between trained and untrained microbiomes. Exercise significantly increased the level of the bacterial species Muribaculaceae bacterium DSM 103720. Computation simulation of bacterial growth was used to predict metabolites that accumulate under in silico culture of exercise‐responsive bacteria. We identified acetate and succinate as potential gut microbial metabolites that are produced by Muribaculaceae bacterium, which were then administered to mice during a period of mechanical overload‐induced muscle hypertrophy. Although no differences were observed for the overall muscle growth response to succinate or acetate administration during the first 5 days of mechanical overload‐induced hypertrophy, acetate and succinate increased skeletal muscle mitochondrial respiration. When given as post‐biotics, succinate or acetate treatment may improve oxidative metabolism during muscle hypertrophy.https://doi.org/10.14814/phy2.15848exercisemetagenomicsmicrobiomeskeletal muscle
spellingShingle Ahmed Ismaeel
Taylor R. Valentino
Benjamin Burke
Jensen Goh
Tolulope P. Saliu
Fatmah Albathi
Allison Owen
John J. McCarthy
Yuan Wen
Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics
Physiological Reports
exercise
metagenomics
microbiome
skeletal muscle
title Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics
title_full Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics
title_fullStr Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics
title_full_unstemmed Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics
title_short Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics
title_sort acetate and succinate benefit host muscle energetics as exercise associated post biotics
topic exercise
metagenomics
microbiome
skeletal muscle
url https://doi.org/10.14814/phy2.15848
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