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Exercise Alters Gut Microbiota Composition and Function in Lean and Obese Humans
Abstract
PURPOSE: Exercise is associated with altered gut microbial composition, but studies have not investigated whether the gut microbiota and associated metabolites are modulated by exercise training in humans. We explored the impact of 6 wk of endurance exercise on the composition, functional capacity, and metabolic output of the gut microbiota in lean and obese adults with multiple-day dietary controls before outcome variable collection. METHODS: Thirty-two lean (n = 18 [9 female]) and obese (n = 14 [11 female]), previously sedentary subjects participated in 6 wk of supervised, endurance-based exercise training (3 d·wk) that progressed from 30 to 60 min·d and from moderate (60% of HR reserve) to vigorous intensity (75% HR reserve). Subsequently, participants returned to a sedentary lifestyle activity for a 6-wk washout period. Fecal samples were collected before and after 6 wk of exercise, as well as after the sedentary washout period, with 3-d dietary controls in place before each collection. RESULTS: β-diversity analysis revealed that exercise-induced alterations of the gut microbiota were dependent on obesity status. Exercise increased fecal concentrations of short-chain fatty acids in lean, but not obese, participants. Exercise-induced shifts in metabolic output of the microbiota paralleled changes in bacterial genes and taxa capable of short-chain fatty acid production. Lastly, exercise-induced changes in the microbiota were largely reversed once exercise training ceased. CONCLUSION: These findings suggest that exercise training induces compositional and functional changes in the human gut microbiota that are dependent on obesity status, independent of diet and contingent on the sustainment of exercise.
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“To date, one study showed that exercise induced compositional changes in the human gut microbiota that were more pronounced in lean than in obese (Allen et al., 2017).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Allen et al., 2017
In the citing paper
“The authors concluded that the shifts were dependent on the obesity status and were reversed after cessation of the training.”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Allen et al., 2017
In the citing paper
“It was recently demonstrated by targeted gene amplification, not metagenomics, that in addition to the influence on the gut microbiota composition, exercise training increased the gene encoding butyrate forming Butyryl CoA: Acetate CoA transferase (Allen et al., 2017)”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Allen et al., 2017
In the citing paper
“while in a human study it increased after cessation of the training and not in response to exercise (Allen et al., 2017).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Allen et al., 2017
In the citing paper
“But interestingly, contradictory findings from the human exercise interventions have been recently presented (Allen et al., 2017; Cronin et al., 2018).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Allen et al., 2017
In the citing paper
“On the other hand, similar to our results, Allen and co-workers reported compositional and β-diversity changes of the microbiota in response to six-weeks endurance training that resembled the intervention of our study (Allen et al., 2017).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Allen et al., 2017
In the citing paper
“Notably, the study also found that a return to sedentary lifestyle for 6 weeks reversed changes in the gut microbiota observed after exercise training, again indicating the sensitivity of the gut microbiome to physical activity.”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [113]
In the citing paper
“Exercise training is a well-known modulator of gut microbiota composition, improving biodiversity and representation of taxa with purported health-promoting significance [26,131].”
From Gut Microbiota, Muscle Mass and Function in Aging: A Focus on Physical Frailty and Sarcopenia (2019) · cites this paper as [131]
In the citing paper
“After the washout period, exercise-induced changes in the microbiota were largely reversed once exercise training ceased.”
From The athletic gut microbiota (2020) · cites this paper as [98]
In the citing paper
“In a longitudinal research design, Allen et al. [98] reported for the first time that exercise training can modulate the composition and metabolic capacity of the human gut microbiota in previously sedentary individuals.”
From The athletic gut microbiota (2020) · cites this paper as [98]
In the citing paper
“Exercise-induced modulations of the gut microbiota and SCFA were strongly associated with changes in body composition in lean participants and VO2max in obese participants, independent of diet.”
From The athletic gut microbiota (2020) · cites this paper as [98]
In the citing paper
“Of note, the exercise induced shifts in SCFA-producing taxa (Faecalibacterium species [spp.] and Lachnospira spp.) and genetic machinery (butyrate-regulating gene, BCoAT) were more substantial in lean versus obese participants.”
From The athletic gut microbiota (2020) · cites this paper as [98]
In the citing paper
“Once these participants ceased training, exercise-induced changes in the microbiota were largely reversed when re-measured after a 6-week sedentary period109.”
From Exerkines in health, resilience and disease (2022) · cites this paper as [109]
In the citing paper
“In humans, chronic exercise altered the gut microbiome to increase availability of short chain fatty acids, particularly butyrate109.”
From Exerkines in health, resilience and disease (2022) · cites this paper as [109]
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Exercise immunology: Future directions
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“Allen et al.179 fol- lowed this up several years later by demonstrating that VWR and FTR have opposing effects on the gut microbiome.”
BackgroundInfluentialInfluence of Exercise on the Human Gut Microbiota of Healthy Adults: A Systematic Review
Ortiz-Alvarez, L., Xu, H., & Martínez‐Téllez, B. (2020) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000126 · Cited by 154
“Four studies (31,38,39,47) used a standardized diet with their subjects before and during the intervention period, but this makes it impossible to know whether the changes seen in the gutmicrobiota were caused by the exercise intervention or the change in diet.”
BackgroundResultInfluentialPhysical activity induced alterations of gut microbiota in humans: a systematic review
Dziewiecka, H., Buttar, H. S., Kasperska, A., Ostapiuk–Karolczuk, J., Domagalska, M., Cichoń-Woźniak, J., & Skarpańska-Stejnborn, A. (2022) · BMC Sports Science Medicine and Rehabilitation · doi:10.1186/s13102-022-00513-2 · Cited by 155
“Further, the enhanced population in the family of Lachnospiraceae or genus Lachnospira confirms the positive impact of moderate-intensity exercise on the gut microbiota [32, 33, 37, 47, 52, 58].”
BackgroundInfluentialKern, T., Blond, M. B., Hansen, T. H., Rosenkilde, M., Quist, J. S., Gram, A. S., Ekstrøm, C. T., Hansen, T., & Stallknecht, B. (2020) · International Journal of Obesity · doi:10.1038/s41366-019-0440-y · Cited by 130
Effects of short‐term endurance exercise on gut microbiota in elderly men
Taniguchi, H., Tanisawa, K., Sun, X., Kubo, T., Hoshino, Y., Hosokawa, M., Takeyama, H., & Higuchi, M. (2018) · Physiological Reports · doi:10.14814/phy2.13935 · Cited by 144
“Recently, it was reported that fecal concentrations of short-chain fatty acids (SCFAs) were increased by 6-week endurance exercise in lean subjects (Allen et al. 2018), and it was suggested that the microbial SCFAs influence blood pressure by interacting with host SCFA receptors (Pluznick 2017).”
BackgroundA Review of the Role of the Gut Microbiome in Personalized Sports Nutrition
Hughes, R. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00191 · Cited by 143
“Related variables, SCFA production and butyrate-producing taxa, have been consistently shown to increase in response to exercise (18, 57, 79) and have also been positively correlated to changes in lean muscle mass, also suggesting that SCFAs may play an important role”
BackgroundInfluentialGut Microbiota Composition Is Related to Cardiorespiratory Fitness in Healthy Young Adults
Durk, R. P., Castillo, E., Márquez-Magaña, L., Grosicki, G. J., Bolter, N. D., Lee, C. M., & Bagley, J. R. (2019) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0024 · Cited by 131
“The observed relationship between cardiorespiratory fitness and gut microbiota composition supports previous research suggesting that exercise training may promote an increase in bacterial strains in the Firmicutes phylum (Allen et al., 2017; Estaki et al., 2016).”
BackgroundResultInfluentialKopczyńska, J., & Kowalczyk, M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1380476 · Cited by 160
Dietary nutrients shape gut microbes and intestinal mucosa via epigenetic modifications
Wu, J., Zhao, Y., Wang, X., Kong, L., Johnston, L. J., Lü, L., & Ma, X. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1828813 · Cited by 132
Sohail, M. U., Yassine, H. M., Sohail, A., & Thani, A. A. A. (2019) · Review of Diabetic Studies · doi:10.1900/rds.2019.15.35 · Cited by 128
“Allen et al . observed that at baseline, the fecal microbiome, microbiome metabolic profile, and cardiorespiratory fitness level of obese subjects were different from those of lean subjects, and exercise training was positively correlated with these parameters [77].”
BackgroundRole of the intestinal microbiome and its therapeutic intervention in cardiovascular disorder
Luqman, A., Hassan, A., Ullah, M., Naseem, S., Ullah, M., Zhang, L., Din, A. U., Ullah, K., Ahmad, W., & Wang, G. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1321395 · Cited by 145
“Research has demonstrated that exercise has the capacity to increase the levels of the bacterial metabolite known as butyrate (279).”
BackgroundCheng, R., Wang, L., Le, S., Yang, Y., Zhao, C., Zhang, X., Yang, X., Xu, T., Xu, L., Wiklund, P., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29968-0 · Cited by 142
Caprara, G. (2021) · Nutrients · doi:10.3390/nu13020429 · Cited by 152
Exploring the gut microbiota: lifestyle choices, disease associations, and personal genomics
Matute, S. P., & Iyavoo, S. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1225120 · Cited by 143
“In the first controlled longitudinal study aimed at evaluating the independent effect of exercise on the gut microbiota, sedentary individuals, lean or with obesity, adopting consistent dietary patterns (110).”
BackgroundNoone, J., Mucinski, J. M., DeLany, J. P., Sparks, L. M., & Goodpaster, B. H. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2023.12.025 · Cited by 128
Mutual Interactions among Exercise, Sport Supplements and Microbiota
Zeppa, S. D., Agostini, D., Gervasi, M., Annibalini, G., Amatori, S., Ferrini, F., Sisti, D., Piccoli, G., Barbieri, E., Sestili, P., et al. (2019) · Nutrients · doi:10.3390/nu12010017 · Cited by 128
“Recently, a positive association between Bacteroides fragilis and childhood obesity and a decrease in Bacteroidetes phylum related to high BMI were reported.”
BackgroundInfluentialDoes Exercise Alter Gut Microbial Composition? A Systematic Review
Mitchell, C. M., Davy, B. M., Hulver, M. W., Neilson, A. P., Bennett, B. J., & Davy, K. P. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001760 · Cited by 120
Ortega, M. A., Fraile‐Μartinez, O., Naya, I., García‐Honduvilla, N., Álvarez‐Mon, M., Buján, J., Asúnsolo, Á., & de la Torre, B. (2020) · Nutrients · doi:10.3390/nu12092749 · Cited by 122
The gut microbiota in osteoarthritis: where do we stand and what can we do?
Hao, X., Shang, X., Liu, J., Chi, R., Zhang, J., & Xu, T. (2021) · Arthritis Research & Therapy · doi:10.1186/s13075-021-02427-9 · Cited by 123
Is There an Exercise-Intensity Threshold Capable of Avoiding the Leaky Gut?
Ribeiro, F. M., Petriz, B. A., Marques, G., Kamilla, L. H., & Franco, O. L. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.627289 · Cited by 119
Maguire, M., & Maguire, G. (2018) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0024 · Cited by 114
Effects of anti-aging interventions on intestinal microbiota
Du, Y., Gao, Y., Zeng, B., Fan, X., Yang, D., & Yang, M. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1994835 · Cited by 118
“Most of the bacterial groups and SCFAs that increased with exercise decreased during a subsequent 6-week sedentary period.(85) Although high-intensity interval training increased insulin sensitivity and cardiovascular fitness, it did not alter the composition of the microbiome.”
BackgroundThe Role of Short-Chain Fatty Acids of Gut Microbiota Origin in Hypertension
Wu, Y., Xu, H., Tu, X., & Gao, Z. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.730809 · Cited by 117
Nuzum, N. D., Loughman, A., Szymlek-Gay, E. A., Hendy, A., Teo, W.-P., & Macpherson, H. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.003 · Cited by 103
Impact of Different Exercise Modalities on the Human Gut Microbiome
Bycura, D. K., Santos, A. C., Shiffer, A., Kyman, S., Winfree, K. N., Sutliffe, J. T., Pearson, T., Sonderegger, D. L., Cope, E. K., & Caporaso, J. G. (2021) · Sports · doi:10.3390/sports9020014 · Cited by 112
“also acutely controlled for dietary consumption by asking subjects to follow a three-day food menu of only foods and drinks reported on a 7-day dietary recall prior to their three fecal sample collections [11].”
BackgroundMethodResultInfluentialThe Role of the Gut Microbiome on Skeletal Muscle Mass and Physical Function: 2019 Update
Lustgarten, M. S. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01435 · Cited by 110
Nay, K., Smiles, W. J., Kaiser, J., McAloon, L. M., Loh, K., Galić, S., Oakhill, J. S., Gundlach, A. L., & Scott, J. W. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084052 · Cited by 112
“As mentioned, exercise increases the relative abundance of taxa-producing SCFAs, in particular butyrate [127,146,147].”
BackgroundImpact of Melatonin on Skeletal Muscle and Exercise
Stacchiotti, A., Favero, G., & Rodella, L. F. (2020) · Cells · doi:10.3390/cells9020288 · Cited by 116
Kulecka, M., Frączek, B., Mikuła, M., Żeber‐Lubecka, N., Karczmarski, J., Paziewska, A., Ambrożkiewicz, F., Jagusztyn-Krynicka, E. K., Cięszczyk, P., & Ostrowski, J. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1758009 · Cited by 107
Tokuhara, D. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.700058 · Cited by 106
Han, M., Yang, K., Yang, P., Zhong, C., Chen, C., Wang, S., Lu, Q., & Ning, K. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1842991 · Cited by 102
Co-Encapsulated Synbiotics and Immobilized Probiotics in Human Health and Gut Microbiota Modulation
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Roles of the gut microbiome in weight management
Carmody, R. N., & Bisanz, J. E. (2023) · Nature Reviews Microbiology · doi:10.1038/s41579-023-00888-0 · Cited by 113
Gut microbiome interventions in human health and diseases
Nie, P., Li, Z., Wang, Y., Zhang, Y., Zhao, M., Luo, J., Du, S., Deng, Z., Chen, J., Wang, Y., et al. (2019) · Medicinal Research Reviews · doi:10.1002/med.21584 · Cited by 94
“It is generally accepted that moderate exercise is beneficial to health, and gut microbiota alterations modulated by exercise have been observed in mice and humans.(221,222) In fact, gut microbiota alterations due to exercise training were recently proven to protect mice from colitis.”
BackgroundSleep Duration and Hypertension: Epidemiological Evidence and Underlying Mechanisms
Bock, J. M., Vungarala, S., Covassin, N., & Somers, V. K. (2021) · American Journal of Hypertension · doi:10.1093/ajh/hpab146 · Cited by 102
Sales, K. M., & Reimer, R. A. (2022) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2022.09.002 · Cited by 106
Exercise effects on cardiovascular disease: from basic aspects to clinical evidence
Sanchis‐Gomar, F., Lavie, C. J., Marín-Puyalto, J., Pérez-Quilis, C., Eijsvogels, T. M. H., O’Keefe, J. H., Perez, M. V., & Blair, S. N. (2021) · Cardiovascular Research · doi:10.1093/cvr/cvab272 · Cited by 109
Vijay, A., Kouraki, A., Gohir, S., Turnbull, J., Kelly, A., Chapman, V., Barrett, D. A., Bulsiewicz, W. J., & Valdes, A. M. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1997559 · Cited by 93
Mills, S., Lane, J. A., Smith, G. J., Grimaldi, K. A., Ross, R. P., & Stanton, C. (2019) · Nutrients · doi:10.3390/nu11071468 · Cited by 88
“, [144] reported that six weeks of endurance exercise increased faecal SCFA concentrations in lean but not obese participants and the metabolic changes were associated with changes in bacterial taxa and genes capable of producing SCFAs.”
BackgroundEffects of domestication on the gut microbiota parallel those of human industrialization
Reese, A. T., Chadaideh, K. S., Diggins, C. E., Schell, L. D., Beckel, M., Callahan, P., Ryan, R., Thompson, M. E., & Carmody, R. N. (2021) · eLife · doi:10.7554/elife.60197 · Cited by 91
Metadata
- Authors
- ALLEN, J. M., MAILING, L. J., NIEMIRO, G. M., MOORE, R., COOK, M. D., WHITE, B. A., HOLSCHER, H. D., & WOODS, J. A.
- Affiliations
- University of Illinois Urbana-Champaign (US)
- ORCID
- Venue
- Medicine & Science in Sports & Exercise
- Published
- 2018-04
- Volume
- 50
- Issue
- 4
- Pages
- 747-757
- ISSN
- 0195-9131 (ISSN-L)
- OpenAlex
- W2770212191
- Semantic Scholar
- 174d28f947e411c5265cc65ec9ba4d74f60b5bc0
- Cited by
- 820
- References
- 42
- Citations by year
- 2026: 121 · 2025: 84 · 2024: 111 · 2023: 106 · 2022: 107 · 2021: 124 · 2020: 85 · 2019: 51 · 2018: 30
- FWCI
- 18.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Medicine & Science in Sports & Exercise (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Illinois at Urbana-Champaign
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- exercise training, gut microbiota, obesity, endurance exercise, short-chain fatty acids, fecal microbiota, beta diversity, sedentary lifestyle
- MeSH terms
- Gastrointestinal Microbiome, Adult, Bacteria, Fatty Acids, Volatile, Feces, Female, Humans, Longitudinal Studies, Male, Obesity, Oxygen Consumption, RNA, Ribosomal, 16S, Exercise, Body Mass Index, Young Adult, Sedentary Behavior
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