Exercise Modifies the Gut Microbiota with Positive Health Effects

Vincenzo Monda, Ines Villano, Antonietta Messina, Anna Valenzano, Teresa Esposito, Fiorenzo Moscatelli, Andrea Viggiano, Giuseppe Cibelli, Sergio Chieffi, Marcellino Monda, Giovanni Messina, Vincenzo Monda, Ines Villano, Antonietta Messina, Anna Valenzano, Teresa Esposito, Fiorenzo Moscatelli, Andrea Viggiano, Giuseppe Cibelli, Sergio Chieffi, Marcellino Monda, Giovanni Messina

Abstract

The human gastrointestinal tract (GIT) is inhabited by a wide cluster of microorganisms that play protective, structural, and metabolic functions for the intestinal mucosa. Gut microbiota is involved in the barrier functions and in the maintenance of its homeostasis. It provides nutrients, participates in the signaling network, regulates the epithelial development, and affects the immune system. Considering the microbiota ability to respond to homeostatic and physiological changes, some researchers proposed that it can be seen as an endocrine organ. Evidence suggests that different factors can determine changes in the gut microbiota. These changes can be both quantitative and qualitative resulting in variations of the composition and metabolic activity of the gut microbiota which, in turn, can affect health and different disease processes. Recent studies suggest that exercise can enhance the number of beneficial microbial species, enrich the microflora diversity, and improve the development of commensal bacteria. All these effects are beneficial for the host, improving its health status. In this paper, we intend to shed some light over the recent knowledge of the role played by exercise as an environmental factor in determining changes in microbial composition and how these effects could provide benefits to health and disease prevention.

Conflict of interest statement

The authors declare that they have no competing interests.

References

    1. Grenham S., Clarke G., Cryan J. F., Dinan T. G. Brain-gut-microbe communication in health and disease. Frontiers in Physiology. 2011;2, article 94:1–15. doi: 10.3389/fphys.2011.00094.
    1. O'Hara A. M., Shanahan F. The gut flora as a forgotten organ. EMBO Reports. 2006;7(7):688–693. doi: 10.1038/sj.embor.7400731.
    1. Adlerberth I., Wold A. E. Establishment of the gut microbiota in Western infants. Acta Paediatrica, International Journal of Paediatrics. 2009;98(2):229–238. doi: 10.1111/j.1651-2227.2008.01060.x.
    1. Eckburg P. B., Bik E. M., Bernstein C. N., et al. Microbiology: diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635–1638. doi: 10.1126/science.1110591.
    1. Bermon S., Petriz B., Kajeniene A., Prestes J., Castell L., Franco O. L. The microbiota: an exercise immunology perspective. Exercise Immunology Review. 2015;21:70–79.
    1. Mackie R. I., Sghir A., Gaskins H. R. Developmental microbial ecology of the neonatal gastrointestinal tract. The American Journal of Clinical Nutrition. 1999;69(5):1035s–1045s.
    1. Payne A. N., Chassard C., Lacroix C. Gut microbial adaptation to dietary consumption of fructose, artificial sweeteners and sugar alcohols: implications for host-microbe interactions contributing to obesity. Obesity Reviews. 2012;13(9):799–809. doi: 10.1111/j.1467-789x.2012.01009.x.
    1. Remely M., Aumueller E., Jahn D., Hippe B., Brath H., Haslberger A. G. Microbiota and epigenetic regulation of inflammatory mediators in type 2 diabetes and obesity. Beneficial Microbes. 2014;5(1):33–43. doi: 10.3920/BM2013.006.
    1. Flint H. J., Scott K. P., Louis P., Duncan S. H. The role of the gut microbiota in nutrition and health. Nature Reviews Gastroenterology & Hepatology. 2012;9(10):577–589. doi: 10.1038/nrgastro.2012.156.
    1. Clarke S. F., Murphy E. F., O'Sullivan O., et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63(12):1913–1920. doi: 10.1136/gutjnl-2013-306541.
    1. Mika A., Van Treuren W., González A., Herrera J. J., Knight R., Fleshner M. 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. 2015;10(5) doi: 10.1371/journal.pone.0125889.e0125889
    1. Gill S. R., Pop M., DeBoy R. T., et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–1359. doi: 10.1126/science.1124234.
    1. Qin J., Li R., Raes J., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65. doi: 10.1038/nature08821.
    1. Conlon M. A., Bird A. R. The impact of diet and lifestyle on gut microbiota and human health. Nutrients. 2015;7(1):17–44. doi: 10.3390/nu7010017.
    1. Bäckhed F., Ley R. E., Sonnenburg J. L., Peterson D. A., Gordon J. I. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915–1920. doi: 10.1126/science.1104816.
    1. Mändar R., Mikelsaar M. Transmission of mother’s microflora to the newborn at birth. Neonatology. 1996;69(1):30–35. doi: 10.1159/000244275.
    1. Palmer C., Bik E. M., DiGiulio D. B., Relman D. A., Brown P. O., Ruan Y. Development of the human infant intestinal microbiota. PLOS Biology. 2007;5(7, article e177) doi: 10.1371/journal.pbio.0050177.
    1. Tannock G. W. What immunologists should know about bacterial communities of the human bowel. Seminars in Immunology. 2007;19(2):94–105. doi: 10.1016/j.smim.2006.09.001.
    1. Nicholson J. K., Holmes E., Kinross J., et al. Host-gut microbiota metabolic interactions. Science. 2012;336(6086):1262–1267. doi: 10.1126/science.1223813.
    1. Ley R. E., Peterson D. A., Gordon J. I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837–848. doi: 10.1016/j.cell.2006.02.017.
    1. Berg R. D. The indigenous gastrointestinal microflora. Trends in Microbiology. 1996;4(11):430–435. doi: 10.1016/0966-842x(96)10057-3.
    1. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229–241. doi: 10.1016/j.cell.2004.07.002.
    1. Vaishnava S., Behrendt C. L., Ismail A. S., Eckmann L., Hooper L. V. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proceedings of the National Academy of Sciences. 2008;105(52):20858–20863. doi: 10.1073/pnas.0808723105.
    1. Mayer L. Mucosal immunity. Pediatrics. 2003;111(6):1595–1600.
    1. Messina G., Dalia C., Tafuri D., et al. Orexin-A controls sympathetic activity and eating behavior. Frontiers in Psychology. 2014;5, article 997 doi: 10.3389/fpsyg.2014.00997.
    1. Sekirov I., Russell S. L., Caetano M Antunes L., Finlay B. B. Gut microbiota in health and disease. Physiological Reviews. 2010;90(3):859–904. doi: 10.1152/physrev.00045.2009.
    1. Akira S., Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family. Immunology Letters. 2003;85(2):85–95. doi: 10.1016/S0165-2478(02)00228-6.
    1. Samuel B. S., Shaito A., Motoike T., et al. 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. 2008;105(43):16767–16772. doi: 10.1073/pnas.0808567105.
    1. Evans J. M., Morris L. S., Marchesi J. R. The gut microbiome: the role of a virtual organ in the endocrinology of the host. Journal of Endocrinology. 2013;218(3):R37–R47. doi: 10.1530/joe-13-0131.
    1. Maslowski K. M., Vieira A. T., Ng A., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461(7268):1282–1286. doi: 10.1038/nature08530.
    1. Viggiano A., Nicodemo U., Viggiano E., et al. Mastication overload causes an increase in O2− production into the subnucleus oralis of the spinal trigeminal nucleus. Neuroscience. 2010;166(2):416–421. doi: 10.1016/j.neuroscience.2009.12.071.
    1. Ley R. E., Bäckhed F., Turnbaugh P., Lozupone C. A., Knight R. D., Gordon J. I. Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(31):11070–11075. doi: 10.1073/pnas.0504978102.
    1. Fava F., Lovegrove J. A., Gitau R., Jackson K. G., Tuohy K. M. The gut microbiota and lipid metabolism: implications for human health and coronary heart disease. Current Medicinal Chemistry. 2006;13(25):3005–3021. doi: 10.2174/092986706778521814.
    1. Wen L., Ley R. E., Volchkov P. Y., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008;455(7216):1109–1113. doi: 10.1038/nature07336.
    1. Viggiano A., Vicidomini C., Monda M., et al. Fast and low-cost analysis of heart rate variability reveals vegetative alterations in noncomplicated diabetic patients. Journal of Diabetes and its Complications. 2009;23(2):119–123. doi: 10.1016/j.jdiacomp.2007.11.009.
    1. Di Bernardo G., Messina G., Capasso S., et al. Sera of overweight people promote in vitro adipocyte differentiation of bone marrow stromal cells. Stem Cell Research & Therapy. 2014;5(1):p. 4.
    1. Frank D. N., St Amand A. L., Feldman R. A., Boedeker E. C., Harpaz N., Pace N. R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(34):13780–13785. doi: 10.1073/pnas.0706625104.
    1. Bäckhed F., Ding H., Wang T., et al. The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(44):15718–15723. doi: 10.1073/pnas.0407076101.
    1. Lichtenstein G. R. Chemokines and cytokines in inflammatory bowel disease and their application to disease treatment. Current Opinion in Gastroenterology. 2000;16(1):83–88. doi: 10.1097/00001574-200001000-00015.
    1. Shanahan F. Probiotics in inflammatory bowel disease—therapeutic rationale and role. Advanced Drug Delivery Reviews. 2004;56(6):809–818. doi: 10.1016/j.addr.2003.11.003.
    1. Macfarlane G. T., Blackett K. L., Nakayama T., Steed H., Macfarlane S. The gut microbiota in inflammatory bowel disease. Current Pharmaceutical Design. 2009;15(13):1528–1536. doi: 10.2174/138161209788168146.
    1. Mawdsley J. E., Rampton D. S. The Role of Psychological Stress in Inflammatory Bowel Disease. Neuroimmunomodulation. 2007;13(5-6):327–336. doi: 10.1159/000104861.
    1. Thompson W. G., Longstreth G. F., Drossman D. A., Heaton K. W., Irvine E. J., Müller-Lissner S. A. Functional bowel disorders and functional abdominal pain. Gut. 1999;45(2):II43–II47.
    1. Quigley E. M. Review: do patients with functional gastrointestinal disorders have an altered gut flora? Therapeutic Advances in Gastroenterology. 2009;2(4):S23–S30. doi: 10.1177/1756283x09335636.
    1. Rajilić-Stojanović M., Biagi E., Heilig H. G. H. J., et al. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology. 2011;141(5):1792–1801. doi: 10.1053/j.gastro.2011.07.043.
    1. Cryan J. F., O'Mahony S. M. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterology and Motility. 2011;23(3):187–192. doi: 10.1111/j.1365-2982.2010.01664.x.
    1. Peters H. P. F., De Vries W. R., Vanberge-Henegouwen G. P., Akkermans L. M. A. Potential benefits and hazards of physical activity and exercise on the gastrointestinal tract. Gut. 2001;48(3):435–439. doi: 10.1136/gut.48.3.435.
    1. Campbell S. C., Wisniewski P. J., Noji M., et al. The effect of diet and exercise on intestinal integrity and microbial diversity in mice. PLoS ONE. 2016;11(3):1–17. doi: 10.1371/journal.pone.0150502.e0150502
    1. Rehrer N. J., Smets A., Reynaert H., Goes E., De Meirleir K. Effect of exercise on portal vein blood flow in man. Medicine and Science in Sports and Exercise. 2001;33(9):1533–1537. doi: 10.1097/00005768-200109000-00017.
    1. Gisolfi C. V. Is the GI system built for exercise? Physiology. 2000;15(3):114–119.
    1. Matsumoto M., Inoue R., Tsukahara T., et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Bioscience, Biotechnology, and Biochemistry. 2008;72(2):572–576. doi: 10.1271/bbb.70474.
    1. Perrin P., Pierre F., Patry Y., et al. Only fibres promoting a stable butyrate producing colonic ecosystem decrease the rate of aberrant crypt foci in rats. Gut. 2001;48(1):53–61. doi: 10.1136/gut.48.1.53.
    1. Evans C. C., LePard K. J., Kwak J. W., et al. Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS ONE. 2014;9(3) doi: 10.1371/journal.pone.0092193.e92193
    1. Queipo-Ortuño M. I., Seoane L. M., Murri M., et al. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS ONE. 2013;8(5) doi: 10.1371/journal.pone.0065465.e65465
    1. Stilling R. M., Ryan F. J., Hoban A. E., et al. Microbes & neurodevelopment—absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala. Brain, Behavior, and Immunity. 2015;50:209–220. doi: 10.1016/j.bbi.2015.07.009.
    1. Diaz Heijtz R., Wang S., Anuar F., et al. Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(7):3047–3052. doi: 10.1073/pnas.1010529108.
    1. Marra L., Cantile M., Scognamiglio G., et al. Deregulation of HOX B13 expression in urinary bladder cancer progression. Current Medicinal Chemistry. 2013;20(6):833–839.
    1. Bravo J. A., Forsythe P., Chew M. V., et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(38):16050–16055. doi: 10.1073/pnas.1102999108.
    1. Forsythe P., Bienenstock J., Kunze W. A. Vagal pathways for microbiome-brain-gut axis communication. Advances in Experimental Medicine and Biology. 2014;817:115–133. doi: 10.1007/978-1-4939-0897-4_5.
    1. Cook M. D., Allen J. M., Pence B. D., et al. Exercise and gut immune function: evidence of alterations in colon immune cell homeostasis and microbiome characteristics with exercise training. Immunology and Cell Biology. 2016;94(2):158–163. doi: 10.1038/icb.2015.108.
    1. Allen J. M., Miller M. E. B., Pence B. D., et al. Voluntary and forced exercise differentially alters the gut microbiome in C57BL/6J Mice. Journal of Applied Physiology. 2015;118(8):1059–1066. doi: 10.1152/japplphysiol.01077.2014.
    1. Petriz B. A., Castro A. P., Almeida J. A., et al. Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats. BMC Genomics. 2014;15, article 511 doi: 10.1186/1471-2164-15-511.
    1. Woo J., Shin K., Park S., Jang K., Kang S. Effects of exercise and diet change on cognition function and synaptic plasticity in high fat diet induced obese rats. Lipids in Health and Disease. 2013;12, article 144 doi: 10.1186/1476-511x-12-144.
    1. Chieffi S., Conson M., Carlomagno S. Movement velocity effects on kinaesthetic localisation of spatial positions. Experimental Brain Research. 2004;158(4):421–426. doi: 10.1007/s00221-004-1916-z.
    1. Molteni R., Wu A., Vaynman S., Ying Z., Barnard R., Gómez-Pinilla F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience. 2004;123(2):429–440. doi: 10.1016/j.neuroscience.2003.09.020.
    1. Chieffi S., Iavarone A., Viggiano A., Monda M., Carlomagno S. Effect of a visual distractor on line bisection. Experimental Brain Research. 2012;219(4):489–498. doi: 10.1007/s00221-012-3106-8.
    1. Li W., Dowd S. E., Scurlock B., Acosta-Martinez V., Lyte M. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiology and Behavior. 2009;96(4-5):557–567. doi: 10.1016/j.physbeh.2008.12.004.
    1. Chieffi S., Iachini T., Iavarone A., Messina G., Viggiano A., Monda M. Flanker interference effects in a line bisection task. Experimental Brain Research. 2014;232(4):1327–1334. doi: 10.1007/s00221-014-3851-y.
    1. Kang S. S., Jeraldo P. R., Kurti A., et al. Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition. Molecular Neurodegeneration. 2014;9, article 36 doi: 10.1186/1750-1326-9-36.
    1. Klaenhammer T., Altermann E., Arigoni F., et al. Lactic Acid Bacteria: Genetics, Metabolism and Applications. Springer Netherlands; 2002. Discovering lactic acid bacteria by genomics; pp. 29–58.
    1. Estaki M., Pither J., Baumeister P., et al. Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. The FASEB Journal. 2016;30(1):1027–1035.
    1. Claesson M. J., Jeffery I. B., Conde S., et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2016;488(7410):178–184. doi: 10.1038/nature11319.
    1. Monda M., Messina G., Scognamiglio I., et al. Short-term diet and moderate exercise in young overweight men modulate cardiocyte and hepatocarcinoma survival by oxidative stress. Oxidative Medicine and Cellular Longevity. 2014;2014:7. doi: 10.1155/2014/131024.131024
    1. Handschin C., Spiegelman B. M. The role of exercise and PGC1α in inflammation and chronic disease. Nature. 2008;454(7203):463–469. doi: 10.1038/nature07206.
    1. Franceschi C., Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2014;69(supplement 1):S4–S9. doi: 10.1093/gerona/glu057.
    1. Chieffi S., Secchi C., Gentilucci M. Deictic word and gesture production: their interaction. Behavioural Brain Research. 2009;203(2):200–206. doi: 10.1016/j.bbr.2009.05.003.
    1. Everard A., Belzer C., Geurts L., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proceedings of the National Academy of Sciences. 2013;110(22):9066–9071. doi: 10.1073/pnas.1219451110.
    1. Juneau M., Hayami D., Gayda M., Lacroix S., Nigam A. Provocative issues in heart disease prevention. Canadian Journal of Cardiology. 2014;30(12):S401–S409. doi: 10.1016/j.cjca.2014.09.014.
    1. Vgontzas A. N. Does obesity play a major role in the pathogenesis of sleep apnoea and its associated manifestations via inflammation, visceral adiposity, and insulin resistance? Archives of Physiology and Biochemistry. 2008;114(4):211–223. doi: 10.1080/13813450802364627.
    1. Tan X., Saarinen A., Mikkola T. M., et al. Effects of exercise and diet interventions on obesity-related sleep disorders in men: study protocol for a randomized controlled trial. Trials. 2013;14(1, article 235) doi: 10.1186/1745-6215-14-235.
    1. Morris G., Berk M., Galecki P., Walder K., Maes M. The neuro-immune pathophysiology of central and peripheral fatigue in systemic immune-inflammatory and neuro-immune diseases. Molecular Neurobiology. 2016;53(2):1195–1219. doi: 10.1007/s12035-015-9090-9.
    1. Maes M. Inflammatory and oxidative and nitrosative stress pathways underpinning chronic fatigue, somatization and psychosomatic symptoms. Current Opinion in Psychiatry. 2009;22(1):75–83. doi: 10.1097/YCO.0b013e32831a4728.
    1. Morris G., Maes M. Oxidative and nitrosative stress and immune-inflammatory pathways in patients with myalgic encephalomyelitis (ME)/chronic fatigue syndrome (CFS) Current Neuropharmacology. 2014;12(2):168–185. doi: 10.2174/1570159X11666131120224653.
    1. Frémont M., Coomans D., Massart S., De Meirleir K. High-throughput 16S rRNA gene sequencing reveals alterations of intestinal microbiota in myalgic encephalomyelitis/chronic fatigue syndrome patients. Anaerobe. 2013;22:50–56. doi: 10.1016/j.anaerobe.2013.06.002.
    1. Chen Y.-M., Wei L., Chiu Y.-S., et al. Lactobacillus plantarum TWK10 supplementation improves exercise performance and increases muscle mass in mice. Nutrients. 2016;8(4):p. 205. doi: 10.3390/nu8040205.
    1. Duncan S. H., Louis P., Flint H. J. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Applied and Environmental Microbiology. 2004;70(10):5810–5817. doi: 10.1128/AEM.70.10.5810-5817.2004.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever