Microbiota influences host exercise capacity via modulation of skeletal muscle glucose metabolism in mice
The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates a...
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Published in | Experimental & molecular medicine Vol. 55; no. 8; pp. 1820 - 1830 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
01.08.2023
Springer Nature B.V Nature Publishing Group |
Subjects | |
Online Access | Get full text |
ISSN | 2092-6413 1226-3613 2092-6413 |
DOI | 10.1038/s12276-023-01063-4 |
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Abstract | The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance.
Gut microbes: unexpected exercise partners
Gut microbes alter metabolism and enhance exercise performance in mice. Gut microbes are known to produce beneficial metabolites and improve health, but how they affect exercise is not well understood. Je Kyung Seong at Seoul National University in South Korea and co-workers compared how mice with a healthy microbiome and germ-free (GF) mice responded to exercise. Although GF mice became exhausted much sooner than non-GF mice, spent one-third less time running, and ate 1.5 times more than non-GF mice, they did not gain weight. Further investigation showed that instead of getting their energy from glucose stored in skeletal muscles, GF mice were burning fat, which reduced their performance; reinstating their gut microbes restored their exercise capacity. A healthy gut microbiome is critical for exercise capacity and future work could focus on identifying key microbial species. |
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AbstractList | The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance.Gut microbes: unexpected exercise partnersGut microbes alter metabolism and enhance exercise performance in mice. Gut microbes are known to produce beneficial metabolites and improve health, but how they affect exercise is not well understood. Je Kyung Seong at Seoul National University in South Korea and co-workers compared how mice with a healthy microbiome and germ-free (GF) mice responded to exercise. Although GF mice became exhausted much sooner than non-GF mice, spent one-third less time running, and ate 1.5 times more than non-GF mice, they did not gain weight. Further investigation showed that instead of getting their energy from glucose stored in skeletal muscles, GF mice were burning fat, which reduced their performance; reinstating their gut microbes restored their exercise capacity. A healthy gut microbiome is critical for exercise capacity and future work could focus on identifying key microbial species. Abstract The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance. The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance. Gut microbes: unexpected exercise partners Gut microbes alter metabolism and enhance exercise performance in mice. Gut microbes are known to produce beneficial metabolites and improve health, but how they affect exercise is not well understood. Je Kyung Seong at Seoul National University in South Korea and co-workers compared how mice with a healthy microbiome and germ-free (GF) mice responded to exercise. Although GF mice became exhausted much sooner than non-GF mice, spent one-third less time running, and ate 1.5 times more than non-GF mice, they did not gain weight. Further investigation showed that instead of getting their energy from glucose stored in skeletal muscles, GF mice were burning fat, which reduced their performance; reinstating their gut microbes restored their exercise capacity. A healthy gut microbiome is critical for exercise capacity and future work could focus on identifying key microbial species. The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance.The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance. The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance. The microbiota enhances exercise performance and regulates host physiology and energy metabolism by producing beneficial metabolites via bacterial fermentation. In this study, we discovered that germ-free (GF) mice had a reduced capacity for aerobic exercise as well as low oxygen consumption rates and glucose availability. Surprisingly, GF mice showed lower body weight gain and lower fat mass than specific pathogen-free (SPF) mice. Therefore, we hypothesized that these paradoxical phenotypes could be mediated by a compensatory increase in lipolysis in adipose tissues owing to impaired glucose utilization in skeletal muscle. Our data revealed that gut microbiota depletion impairs host aerobic exercise capacity via the deterioration of glucose storage and utilization. The improved browning ability of GF mice may have contributed to the lean phenotype and negatively affected energy generation. These adaptations limit obesity in GF mice but impede their immediate fuel supply during exercise, resulting in decreased exercise performance. Gut microbes alter metabolism and enhance exercise performance in mice. Gut microbes are known to produce beneficial metabolites and improve health, but how they affect exercise is not well understood. Je Kyung Seong at Seoul National University in South Korea and co-workers compared how mice with a healthy microbiome and germ-free (GF) mice responded to exercise. Although GF mice became exhausted much sooner than non-GF mice, spent one-third less time running, and ate 1.5 times more than non-GF mice, they did not gain weight. Further investigation showed that instead of getting their energy from glucose stored in skeletal muscles, GF mice were burning fat, which reduced their performance; reinstating their gut microbes restored their exercise capacity. A healthy gut microbiome is critical for exercise capacity and future work could focus on identifying key microbial species. |
Author | Kim, Hye Jin Kim, Hak Su Baek, Ji Hyeon Kim, Youn Ju Kim, Yong Jae Kim, Il Yong Seong, Je Kyung |
Author_xml | – sequence: 1 givenname: Hye Jin surname: Kim fullname: Kim, Hye Jin organization: Laboratory of Developmental Biology and Genomics, Research Institute for Veterinary Science, College of Veterinary Medicine, Seoul National University, Korea Mouse Phenotyping Center (KMPC), Seoul National University – sequence: 2 givenname: Youn Ju surname: Kim fullname: Kim, Youn Ju organization: Laboratory of Developmental Biology and Genomics, Research Institute for Veterinary Science, College of Veterinary Medicine, Seoul National University, Korea Mouse Phenotyping Center (KMPC), Seoul National University, BK21 Program for Veterinary Science, College of Veterinary Medicine, Seoul National University – sequence: 3 givenname: Yong Jae surname: Kim fullname: Kim, Yong Jae organization: Korea Mouse Phenotyping Center (KMPC), Seoul National University – sequence: 4 givenname: Ji Hyeon surname: Baek fullname: Baek, Ji Hyeon organization: Korea Mouse Phenotyping Center (KMPC), Seoul National University – sequence: 5 givenname: Hak Su surname: Kim fullname: Kim, Hak Su organization: Korea Mouse Phenotyping Center (KMPC), Seoul National University – sequence: 6 givenname: Il Yong surname: Kim fullname: Kim, Il Yong organization: Laboratory of Developmental Biology and Genomics, Research Institute for Veterinary Science, College of Veterinary Medicine, Seoul National University, Korea Mouse Phenotyping Center (KMPC), Seoul National University – sequence: 7 givenname: Je Kyung orcidid: 0000-0003-1177-6958 surname: Seong fullname: Seong, Je Kyung email: snumouse@snu.ac.kr organization: Laboratory of Developmental Biology and Genomics, Research Institute for Veterinary Science, College of Veterinary Medicine, Seoul National University, Korea Mouse Phenotyping Center (KMPC), Seoul National University, BK21 Program for Veterinary Science, College of Veterinary Medicine, Seoul National University, Interdisciplinary Program for Bioinformatics, Program for Cancer Biology and BIO-MAX/N-Bio Institute, Seoul National University |
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SubjectTerms | 13/1 13/51 631/443/319/1557 631/443/319/1642/2037 64/60 82/80 Adipose tissue Aerobic capacity Aerobics Animal models Biomedical and Life Sciences Biomedicine Body fat Body weight gain Energy metabolism Exercise Fermentation Germfree Glucose Glucose metabolism Intestinal microflora Lipolysis Medical Biochemistry Metabolism Metabolites Microbiomes Microbiota Molecular Medicine Musculoskeletal system Oxygen consumption Phenotypes Physical fitness Physical training Skeletal muscle Specific pathogen free Stem Cells |
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Title | Microbiota influences host exercise capacity via modulation of skeletal muscle glucose metabolism in mice |
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