Physical activity regulates the intestinal microbiota composition

Authors

  • Mihaela Jurdana University of Primorska, Faculty of Health Sciences
  • Darja Barlič-Maganja University of Primorska, Faculty of Health Sciences

DOI:

https://doi.org/10.35469/ak.2019.185

Keywords:

gut microbiota, physical exercise, health

Abstract

Gut microbiota is the name given today to the bacterial population living in our intestine. It provides nutrients, metabolites and affects the immune system. Recent animals and human studies suggest that regular physical activity increases the presence of beneficial microbial species of gut microbiota and improves the health status of the host. When gut bacteria diversity reduces, there are systemic consequences leading to gastrointestinal, physiological and psychological distress. This review describes the communication pathway of the microbiota-gut-brain axes and other possible mechanisms by which physical activity causes changes in microbiota composition. Furthermore, it provides the latest evidence of the beneficial role of exercise, which in turn can affect health and various disease processes. The results of research studies in this area are increasingly becoming a focus of scientific attention.

References

Aagaard, K., Ma, J., Antony, K. M., Ganu, R., Petrosino, J., & Versalovic, J. (2014). The placenta harbors a unique microbiome. Science Translational Medicine, 6(237), 237ra65. https://doi.org/10.1126/scitranslmed.3008599

Akira, S., & Hemmi, H. (2003). Recognition of pathogen-associated molecular patterns by TLR family. Immunology Letters, 85(2), 85–95. https://doi.org/10.1016/S0165-2478(02)00228-6

Arora, T., & Bäckhed, F. (2016). The gut microbiota and metabolic disease: current understanding and future perspectives. Journal of Internal Medicine, 280(4), 339-349. https://doi.org/10.1111/joim.12508

Allen, J. M., Mailing, L. J., Cohrs, J., Salmonson, C., Fryer, J. D., Nehra, V., ... Woods, J. A. (2018). Exercise training-induced modification of the gut microbiota persists after microbiota colonization and attenuates the response to chemically-induced colitis in gnotobiotic mice. Gut Microbes, 9(2), 115–130. https://doi.org/10.1080/19490976.2017.1372077

Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., & Gordon, J. I. (2005). Host-bacterial mutualism in the human intestine. Science, 307(5717), 1915–1920. https://doi.org/10.1126/science.1104816

Bercik, P., Park, A. J., Sinclair, D., Khoshdel, A., Lu, J., Huang, X., … Verdu, E. F. (2011). The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterology and motility: the official journal of the European Gastrointestinal Motility Society, 23(12), 1132–1139. https://doi.org/10.1111/j.1365-2982.2011.01796.x

Bhagavata Srinivasan, S. P., Raipuria, M., Bahari, H., Kaakoush, N. O., & Morris, M. J. (2018). Impacts of diet and exercise on maternal gut microbiota are transferred to offspring. Frontiers in Endocrinology, 9, 716. https://doi.org/10.3389/fendo.2018.00716

Bokulich, N. A., Chung, J., Battaglia, T., Henderson, N., Jay, M., Li, H., ... Blaser, M. J. (2016). Antibiotics, birth mode, and diet shape microbiome maturation during early life. Science Translational Medicine, 8(343), 343ra82. https://doi.org/10.1126/scitranslmed.aad7121

Choi, J. J., Eum, S. Y., Rampersaud, E., Daunert, S., Abreu, M. T., & Toborek, M. (2013). Exercise attenuates PCB-induced changes in the mouse gut microbiome. Environmental Health Perspectives, 121(6), 725–730. https://doi.org/10.1289/ehp.1306534

Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O'Connor, E. M., Cusack, S., … O’Toole, P. W. (2012). Gut microbiota composition correlates with diet and health in the elderly. Nature, 488(7410), 178-184. https://doi.org/10.1038/nature11319

Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R., Shanahan, F., …Cryan, J. F. (2013). The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Molecular Psychiatry, 18(6), 666-673. https://doi.org/10.1038/mp.2012.77

Clarke, S. F., Murphy, E. F., O'Sullivan, O., Lucey, A. J., Humphreys, M., Hogan, A., ... Cotter, P. D. (2014). Exercise and associated dietary extremes impact on gut microbial diversity. Gut, 63(12), 1913-1920. https://doi.org/10.1136/gutjnl-2013-306541

Clemente, J. C., Ursell, L. K., Parfrey, L. W., & Knight, R. (2012). The impact of the gut microbiota on human health: an integrative view. Cell, 148(6), 1258-1270. https://doi.org/10.1016/j.cell.2012.01.035

Colcombe, S. J., Erickson, K. I., Scalf, P. E., Kim, J. S., Prakash, R., McAuley, E., … Kramer, A. F. (2006). Aerobic exercise training increases brain volume in aging humans. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 61(11), 1166–1170. https://doi.org/10.1093/gerona/61.11.1166

Cook, M. D., Allen, J. M., Pence, B. D., Wallig, M. A., Gaskins, H. R., White, B. A., & Woods, J. A. (2016). Exercise and gut immune function: evidence of alterations in colon immune cell homeostasis and microbiome characteristics with exercise training. Immunology and Cell Biology, 94(2), 158-163. https://doi.org/10.1038/icb.2015.108

Cryan, J. F., & Dinan, T. G. (2012). Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nature Reviews Neuroscience, 13(10), 701-712. https://doi.org/10.1038/nrn3346

Dalton, A., Mermier, C., & Zuhl, M. (2019). Exercise influence on the microbiome-gut-brain axis. Gut Microbes, 10(5), 555-568. https://doi.org/10.1080/19490976.2018.1562268.

Dieterich, W., Schink, M., & Zopf, Y. (2018). Microbiota in the gastrointestinal tract. Medical Sciences (Basel, Switzerland), 6(4), 116. https://doi.org/10.3390/medsci6040116

Dokladny, K., Zuhl, M. N., & Moseley, P. L. (2015). Intestinal epithelial barrier function and tight junction proteins with heat and exercise. Journal of Applied Physiology, 120(6), 692–701. https://doi.org/10.1152/japplphysiol.00536.2015

Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent M., ... Relman, D. A. (2005). Diversity of the human intestinal microbial flora. Science, 308(5728), 1635-1638. https://doi.org/10.1126/science.1110591

Estaki, M., Pither, J., Baumeister, P., Little, J. P., Gill, S. K., Ghosh, S., ... Gibson, D. L. (2016). Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. Microbiome, 4(1), 42. https://doi.org/10.1186/s40168-016-0189-7

Evans, J. M., Morris, L. S., & Marchesi, J. R. (2013). The gut microbiome: the role of a virtual organ in the endocrinology of the host. Journal of Endocrinology, 218(3), R37–R47. https://doi.org/10.1530/joe-13-0131

Farzi, A., Fröhlich, E. E., & Holzer, P. (2018). Gut microbiota and the neuroendocrine system. Neurotherapeutics: the Journal of the American Society for Experimental NeuroTherapeutics, 15(1), 5–22. https://doi.org/10.1007/s13311-017-0600-5

Flint, H. J., Scott, K. P., Louis, P., & Duncan, S. H. (2012). The role of the gut microbiota in nutrition and health. Nature Reviews Gastroenterology & Hepatology, 9(10), 577–589. https://doi.org/10.1038/nrgastro.2012.156

Forsythe, P., Kunze, W. A., & Bienenstock, J. (2012). On communication between gut microbes and the brain. Current Opinion in Gastroenterology, 28(6), 557–562. https://doi.org/10.1097/MOG.0b013e3283572ffa

Forsythe, P., Kunze, W., & Bienenstock, J. (2016). Moody microbes or fecal phrenology: what do we know about the microbiota-gut-brain axis? BMC Medicine, 14, 58. https://doi.org/10.1186/s12916-016-0604-8

Garrett, W. S. (2015). Cancer and the microbiota. Science, 348(6230), 80-86. https://doi.org/10.1126/science.aaa4972

Ghaisas, S., Maher, J., & Kanthasamy, A. (2016). Gut microbiome in health and disease: linking the microbiome-gut-brain axis and environmental factors in the pathogenesis of systemic and neurodegenerative diseases. Pharmacology & Therapeutics, 158, 52-62. https://doi.org/10.1016/j.pharmthera.2015.11.012

Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011). Brain-gut-microbe communication in health and disease. Frontiers in Physiology, 2, 94. https://doi.org/10.3389/fphys.2011.00094

Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., ... Mazmanian, S. K. (2013). Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 155(7), 1451–1463. https://doi.org/10.1016/j.cell.2013.11.024

Jackson, M. A., Jeffery, I. B., Beaumont, M., Bell J. T., Clark, A. G., Ley, R. E., ... Steves, C. J. (2016). Signatures of early frailty in the gut microbiota. Genome Medicine, 8(1), 8. https://doi.org/10.1186/s13073-016-0262-7

Jenkins, T. A., Nguyen, J. C., Polglaze, K. E., & Bertrand, P. P. (2016). Influence of tryptophan and serotonin on mood and cognition with a possible role of the gut-brain axis. Nutrients, 8(1), 56. https://doi.org/10.3390/nu8010056

Juneau, M., Hayami, D., Gayda, M., Lacroix, S., & Nigam, A. (2014). Provocative issues in heart disease prevention. Canadian Journal of Cardiology, 30(12 Suppl), S401-409. https://doi.org/10.1016/j.cjca.2014.09.014

Kashtanova, D. A., Popenko, A. S., Tkacheva, O. N., Tyakht, A. B., Alexeev, D. G., & Boytsov, S. A. (2016). Association between the gut microbiota and diet: fetal life, early childhood, and further life. Nutrition, 32(6), 620-627. https://doi.org/10.1016/j.nut.2015.12.037

Kim, Y. K., & Shin, C. (2018). The microbiota-gut-brain axis in neuropsychiatric disorders: pathophysiological mechanisms and novel treatments. Current Neuropharmacology, 16(5), 559-573. https://doi.org/10.2174/1570159X15666170915141036

Knauf, F., Brewer, J. R., & Flavell, R. A. (2019). Immunity, microbiota and kidney disease. Nature Reviews Nephrology, 15, 263–274. https://doi.org/10.1038/s41581-019-0118-7

Kriss, M., Hazleton, K. Z., Nusbacher, N. M., Martin, C. G., & Lozupone, C. A. (2018). Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. Current Opinion in Microbiology, 44, 34-40. https://doi.org/10.1016/j.mib.2018.07.003

Levy, M., Kolodziejczyk, A. A., Thaiss, C. A., & Elinav, E. (2017). Dysbiosis and the immune system. Nature Reviews Immunology, 17(4), 219-232. https://doi.org/10.1038/nri.2017.7

Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D., Hirschfield, G. M., Hold, G., ... Hart, A. (2016). The gut microbiota and host health: a new clinical frontier. Gut, 65(2), 330-339. https://doi.org/10.1136/gutjnl-2015-309990

Matsumoto, M., Inoue, R., Tsukahara, T., Ushida, K., Chiji, H., Matsubara, N., & Hara, H. (2008). Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Bioscience, Biotechnology and Biochemistry, 72(2), 572–576. https://doi.org/10.1271/bbb.70474

McKenzie, C., Tan, J., Macia, L., & Mackay, C. R. (2017). The nutrition-gut microbiome-physiology axis and allergic diseases. Immunology Reviews, 278(1), 277-295. https://doi.org/10.1111/imr.12556

Mika, A., Van Treuren, W., González, A., Herrera, J. J., Knight, R., & Fleshner, M. (2015). Exercise is more effective at altering gut microbial composition and producing stable changes in lean mass in juvenile versus adult male F344 rats. PloS one, 10(5), e0125889. https://doi.org/10.1371/journal.pone.0125889

Milani, C., Duranti, S., Bottacini, F., Casey, E., Turroni, F., Mahony, J., ... Ventura, M. (2017). The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota. Microbiology and Molecular Biology Reviews, 81(4), e00036-17. https://doi.org/10.1128/MMBR.00036-17

Milani, C., Ferrario, C., Turroni, F., Duranti, S., Mangifesta, M., van Sinderen, D., & Ventura, M. (2016). The human gut microbiota and its interactive connections to diet. Journal of Human Nutrition and Dietetics, 29(5), 539-546. https://doi.org/10.1111/jhn.12371

Monda, V., Villano, I., Messina, A., Valenzano, A., Esposito, T., Moscatelli, F., ... Messina, G. (2017). Exercise modifies the gut microbiota with positive health effects. Oxidative Medicine and Cellular Longevity, 2017, 3831972. https://doi.org/10.1155/2017/3831972

Murtaza, N., Burke, L. M., Vlahovich, N., Charlesson, B., O’ Neill, H., Ross, M. L., ... Morrison, M. (2019). The effects of dietary pattern during intensified training on stool microbiota of elite race walkers. Nutrients, 11(2), 261. https://doi.org/10.3390/nu11020261

Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012). Host-gut microbiota metabolic interactions. Science, 336(6086), 1262–1267. https://doi.org/10.1126/science.1223813

O’Hara, A. M., & Shanahan, F. (2006). The gut flora as a forgotten organ. EMBO Reports, 7(7), 688–693. https://doi.org/10.1038/sj.embor.7400731

Ohlsson, C., & Sjögren, K. (2015). Effects of the gut microbiota on bone mass. Trends in Microbiology, 26(2), 69-74. https://doi.org/10.1016/j.tem.2014.11.004

O’Mahony, S., Clarke, G., Borre, Y., Dinan, T. & Cryan, J. (2015). Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behavioural Brain Research, 277, 32–48. https://doi.org/10.1016/j.bbr.2014.07.027

Petersen, L. M., Bautista, E. J., Nguyen, H., Hanson, B. M., Chen, L., Lek, S. H., ... Weinstock, G. M. (2017). Community characteristics of the gut microbiomes of competitive cyclists. Microbiome, 5(1), 98. https://doi.org/10.1186/s40168-017-0320-4

Proctor, C., Thiennimitr, P., Chattipakorn, N., & Chattipakorn, S. C. (2017). Diet, gut microbiota and cognition. Metabolic Brain Disease, 32(1), 1–17. https://doi.org/10.1007/s11011-016-9917-8

Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., ... Li, L. (2014). Alterations of the human gut microbiome in liver cirrhosis. Nature, 513(7516), 59-64. https://doi.org/10.1038/nature13568

Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., & Medzhitov, R. (2004). Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell, 118(2), 229–241. https://doi.org/10.1016/j.cell.2004.07.002

Rodriguez, J. M., Murphy, K., Stanton, C., Ross, R. P., Kober, O. I., Juge, N., Collado, M. C. (2015). The composition of the gut microbiota throughout life, with an emphasis on early life. Microbial Ecology in Health and Disease, 26(2), 26050, https://doi.org/10.3402/mehd.v26.26050

Samuel, B. S., Shaito, A., Motoike, T., Rey, F. E., Backhed, F., Manchester, J. K., ... Gordon, J. I. (2008). Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proceedings of the National Academy of Sciences of the United States of America, 105(43), 16767–16772. https://doi.org/10.1073/pnas.0808567105

Schmidt, T. S. B., Raes, J., & Bork, P. (2018). The human gut microbiome: from association to modulation. Cell, 172(6), 1198-1215. https://doi.org/10.1016/j.cell.2018.02.044

Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X. N., … Koga, Y. (2004). Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. The Journal of Physiology, 558(1), 263–275. https://doi.org/10.1113/jphysiol.2004.063388

Tan, X., Saarinen, A., Mikkola, T. M., Tenhunen, J., Martinmäki, S., Rahikainen, A., … Cheng, S. (2013). Effects of exercise and diet interventions on obesity-related sleep disorders in men: study protocol for a randomized controlled trial. Trials, 14, 235. https://doi.org/10.1186/1745-6215-14-235

Tanaka, M., & Nakayama, J. (2017). Development of the gut microbiota in infancy and its impact on health in later life. Allergology International, 66(4), 515-522. https://doi.org/10.1016/j.alit.2017.07.010

Taniguchi, H., Tanisawa, K., Sun, X., Kubo, T., Hoshino, Y., Hosokawa, … Higuchi, M. (2018). Effects of short-term endurance exercise on gut microbiota in elderly men. Physiological Reports, 6(23), e13935. https://doi.org/10.14814/phy2.13935

Ticinesi, A., Lauretani, F., Tana, C., Nouvenne, A., Ridolo, E., & Meschi, T. (2019). Exercise and immune system as modulators of intestinal microbiome: implications for the gut-muscle axis hypothesis. Exercise Immunology Review, 25, 84-95. Retrieved from: http://eir-isei.de/2019/eir-2019-084-article.pdf

Tsigos, C. & Chrousos, G. P. (2002). Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. The Journal of Psychosomatic Research, 53(4), 865–871. https://doi.org/10.1016/S0022-3999(02)00429-4

Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444(7122), 1027-1031. https://doi.org/10.1038/nature05414

Vaishnava, S., Behrendt, C. L., Ismail, A. S., Eckmann, L., & Hooper, L. V. (2008). Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proceedings of the National Academy of Sciences, 105(52), 20858–20863. https://doi.org/10.1073/pnas.0808723105

Walsh, N. P., Gleeson, M., Shephard, R. J., Gleeson, M., Woods, J. A., Bishop, N. C., … Simon, P. (2011). Position statement. Part one: Immune function and exercise. Exercise Immunology Review, 17, 6-63. Retrieved from: http://eir-isei.de/2011/eir-2011-006-article.pdf

Welly, R. J., Liu, T. W., Zidon, T. M., Rowles, J. L., Park, Y. M., Smith, T. N., … Vieira-Potter, V. (2016). Comparison of diet vs. exercise on metabolic function & gut microbiota in obese rats. Medicine & Science in Sports & Exercise, 48(9), 1688-1698. https://doi.org/10.1249/MSS.0000000000000964

Yano, J. M., Yu, K., Donaldson, G. P., Shastri, G. G., Ann, P., Ma, L., … Hsiao, E. Y. (2015). Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell, 161(2), 264–276. https://doi.org/10.1016/j.cell.2015.02.047

Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., … Gordon, J. I. (2012). Human gut microbiome viewed across age and geography. Nature, 486(7402), 222–227. https://doi.org/10.1038/nature11053

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Published

25-11-2019

How to Cite

Jurdana, M., & Barlič-Maganja, D. (2019). Physical activity regulates the intestinal microbiota composition. Annales Kinesiologiae, 10(2), 99–114. https://doi.org/10.35469/ak.2019.185