The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes
Abstract Background The gut microbiome regulates host energy balance and adiposity-related metabolic consequences, but it remains unknown how the gut microbiome modulates body weight response to physical activity (PA). Methods Nested in the Health Professionals Follow-up Study, a subcohort of 307 he...
| Main Authors: | , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | Microbiome |
| Online Access: | https://doi.org/10.1186/s40168-023-01542-w |
| _version_ | 1797811319896801280 |
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| author | Kai Wang Raaj S. Mehta Wenjie Ma Long H. Nguyen Dong D. Wang Andrew R. Ghazi Yan Yan Laila Al-Shaar Yiqing Wang Dong Hang Benjamin C. Fu Shuji Ogino Eric B. Rimm Frank B. Hu Rachel N. Carmody Wendy S. Garrett Qi Sun Andrew T. Chan Curtis Huttenhower Mingyang Song |
| author_facet | Kai Wang Raaj S. Mehta Wenjie Ma Long H. Nguyen Dong D. Wang Andrew R. Ghazi Yan Yan Laila Al-Shaar Yiqing Wang Dong Hang Benjamin C. Fu Shuji Ogino Eric B. Rimm Frank B. Hu Rachel N. Carmody Wendy S. Garrett Qi Sun Andrew T. Chan Curtis Huttenhower Mingyang Song |
| author_sort | Kai Wang |
| collection | DOAJ |
| description | Abstract Background The gut microbiome regulates host energy balance and adiposity-related metabolic consequences, but it remains unknown how the gut microbiome modulates body weight response to physical activity (PA). Methods Nested in the Health Professionals Follow-up Study, a subcohort of 307 healthy men (mean[SD] age, 70[4] years) provided stool and blood samples in 2012–2013. Data from cohort long-term follow-ups and from the accelerometer, doubly labeled water, and plasma biomarker measurements during the time of stool collection were used to assess long-term and short-term associations of PA with adiposity. The gut microbiome was profiled by shotgun metagenomics and metatranscriptomics. A subcohort of 209 healthy women from the Nurses’ Health Study II was used for validation. Results The microbial species Alistipes putredinis was found to modify the association between PA and body weight. Specifically, in individuals with higher abundance of A. putredinis, each 15-MET-hour/week increment in long-term PA was associated with 2.26 kg (95% CI, 1.53–2.98 kg) less weight gain from age 21 to the time of stool collection, whereas those with lower abundance of A. putredinis only had 1.01 kg (95% CI, 0.41–1.61 kg) less weight gain (p interaction = 0.019). Consistent modification associated with A. putredinis was observed for short-term PA in relation to BMI, fat mass%, plasma HbA1c, and 6-month weight change. This modification effect might be partly attributable to four metabolic pathways encoded by A. putredinis, including folate transformation, fatty acid β-oxidation, gluconeogenesis, and stearate biosynthesis. Conclusions A greater abundance of A. putredinis may strengthen the beneficial association of PA with body weight change, suggesting the potential of gut microbial intervention to improve the efficacy of PA in body weight management. Video Abstract |
| first_indexed | 2024-03-13T07:21:56Z |
| format | Article |
| id | doaj.art-24fca15c19df4c6493f75b0208cf0cfb |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-13T07:21:56Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-24fca15c19df4c6493f75b0208cf0cfb2023-06-04T11:34:17ZengBMCMicrobiome2049-26182023-05-0111111710.1186/s40168-023-01542-wThe gut microbiome modifies the associations of short- and long-term physical activity with body weight changesKai Wang0Raaj S. Mehta1Wenjie Ma2Long H. Nguyen3Dong D. Wang4Andrew R. Ghazi5Yan Yan6Laila Al-Shaar7Yiqing Wang8Dong Hang9Benjamin C. Fu10Shuji Ogino11Eric B. Rimm12Frank B. Hu13Rachel N. Carmody14Wendy S. Garrett15Qi Sun16Andrew T. Chan17Curtis Huttenhower18Mingyang Song19Department of Epidemiology, Harvard T.H. Chan School of Public HealthClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical SchoolClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical SchoolClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical SchoolHarvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public HealthBroad Institute of MIT and HarvardDepartment of Biostatistics, Harvard T.H. Chan School of Public HealthDepartment of Nutrition, Harvard T.H. Chan School of Public HealthClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical SchoolDepartment of Nutrition, Harvard T.H. Chan School of Public HealthDepartment of Epidemiology, Harvard T.H. Chan School of Public HealthDepartment of Epidemiology, Harvard T.H. Chan School of Public HealthDepartment of Epidemiology, Harvard T.H. Chan School of Public HealthDepartment of Epidemiology, Harvard T.H. Chan School of Public HealthHarvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public HealthHarvard Chan Microbiome in Public Health Center, Harvard T.H. Chan School of Public HealthDepartment of Epidemiology, Harvard T.H. Chan School of Public HealthClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical SchoolBroad Institute of MIT and HarvardDepartment of Epidemiology, Harvard T.H. Chan School of Public HealthAbstract Background The gut microbiome regulates host energy balance and adiposity-related metabolic consequences, but it remains unknown how the gut microbiome modulates body weight response to physical activity (PA). Methods Nested in the Health Professionals Follow-up Study, a subcohort of 307 healthy men (mean[SD] age, 70[4] years) provided stool and blood samples in 2012–2013. Data from cohort long-term follow-ups and from the accelerometer, doubly labeled water, and plasma biomarker measurements during the time of stool collection were used to assess long-term and short-term associations of PA with adiposity. The gut microbiome was profiled by shotgun metagenomics and metatranscriptomics. A subcohort of 209 healthy women from the Nurses’ Health Study II was used for validation. Results The microbial species Alistipes putredinis was found to modify the association between PA and body weight. Specifically, in individuals with higher abundance of A. putredinis, each 15-MET-hour/week increment in long-term PA was associated with 2.26 kg (95% CI, 1.53–2.98 kg) less weight gain from age 21 to the time of stool collection, whereas those with lower abundance of A. putredinis only had 1.01 kg (95% CI, 0.41–1.61 kg) less weight gain (p interaction = 0.019). Consistent modification associated with A. putredinis was observed for short-term PA in relation to BMI, fat mass%, plasma HbA1c, and 6-month weight change. This modification effect might be partly attributable to four metabolic pathways encoded by A. putredinis, including folate transformation, fatty acid β-oxidation, gluconeogenesis, and stearate biosynthesis. Conclusions A greater abundance of A. putredinis may strengthen the beneficial association of PA with body weight change, suggesting the potential of gut microbial intervention to improve the efficacy of PA in body weight management. Video Abstracthttps://doi.org/10.1186/s40168-023-01542-w |
| spellingShingle | Kai Wang Raaj S. Mehta Wenjie Ma Long H. Nguyen Dong D. Wang Andrew R. Ghazi Yan Yan Laila Al-Shaar Yiqing Wang Dong Hang Benjamin C. Fu Shuji Ogino Eric B. Rimm Frank B. Hu Rachel N. Carmody Wendy S. Garrett Qi Sun Andrew T. Chan Curtis Huttenhower Mingyang Song The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes Microbiome |
| title | The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes |
| title_full | The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes |
| title_fullStr | The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes |
| title_full_unstemmed | The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes |
| title_short | The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes |
| title_sort | gut microbiome modifies the associations of short and long term physical activity with body weight changes |
| url | https://doi.org/10.1186/s40168-023-01542-w |
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