The athletic gut microbiota

Alex E Mohr, Ralf Jäger, Katie C Carpenter, Chad M Kerksick, Martin Purpura, Jeremy R Townsend, Nicholas P West, Katherine Black, Michael Gleeson, David B Pyne, Shawn D Wells, Shawn M Arent, Richard B Kreider, Bill I Campbell, Laurent Bannock, Jonathan Scheiman, Craig J Wissent, Marco Pane, Douglas S Kalman, Jamie N Pugh, Carmen P Ortega-Santos, Jessica A Ter Haar, Paul J Arciero, Jose Antonio, Alex E Mohr, Ralf Jäger, Katie C Carpenter, Chad M Kerksick, Martin Purpura, Jeremy R Townsend, Nicholas P West, Katherine Black, Michael Gleeson, David B Pyne, Shawn D Wells, Shawn M Arent, Richard B Kreider, Bill I Campbell, Laurent Bannock, Jonathan Scheiman, Craig J Wissent, Marco Pane, Douglas S Kalman, Jamie N Pugh, Carmen P Ortega-Santos, Jessica A Ter Haar, Paul J Arciero, Jose Antonio

Abstract

The microorganisms in the gastrointestinal tract play a significant role in nutrient uptake, vitamin synthesis, energy harvest, inflammatory modulation, and host immune response, collectively contributing to human health. Important factors such as age, birth method, antibiotic use, and diet have been established as formative factors that shape the gut microbiota. Yet, less described is the role that exercise plays, particularly how associated factors and stressors, such as sport/exercise-specific diet, environment, and their interactions, may influence the gut microbiota. In particular, high-level athletes offer remarkable physiology and metabolism (including muscular strength/power, aerobic capacity, energy expenditure, and heat production) compared to sedentary individuals, and provide unique insight in gut microbiota research. In addition, the gut microbiota with its ability to harvest energy, modulate the immune system, and influence gastrointestinal health, likely plays an important role in athlete health, wellbeing, and sports performance. Therefore, understanding the mechanisms in which the gut microbiota could play in the role of influencing athletic performance is of considerable interest to athletes who work to improve their results in competition as well as reduce recovery time during training. Ultimately this research is expected to extend beyond athletics as understanding optimal fitness has applications for overall health and wellness in larger communities. Therefore, the purpose of this narrative review is to summarize current knowledge of the athletic gut microbiota and the factors that shape it. Exercise, associated dietary factors, and the athletic classification promote a more "health-associated" gut microbiota. Such features include a higher abundance of health-promoting bacterial species, increased microbial diversity, functional metabolic capacity, and microbial-associated metabolites, stimulation of bacterial abundance that can modulate mucosal immunity, and improved gastrointestinal barrier function.

Keywords: Athletes; Exercise; Gut health; Gut microbiome; Metagenome; Microbial ecology; Physical activity; Short-chain fatty acids; Sport performance; Sports nutrition.

Conflict of interest statement

KB, LB, and SDW declare no competing interests. RJ has received grants to evaluate the efficacy and safety of probiotics, serves on scientific advisory boards, and has served as an expert witness, legal and scientific consultant. AEM and KCC are employed by Isagenix, a company selling branded probiotics products. CMK has previously received external funding to conduct research studies involving nutritional supplements and is currently conducting studies involving prebiotics and probiotics. MP has received grants to evaluate the efficacy and safety of probiotics and has served as a scientific consultant. JRT reports no conflicts of interest regarding the material or paper presented. JRT has previously received grants to evaluate the efficacy of various nutritional supplements including probiotics. NPW reports no conflicts of interested regarding the paper presented and has been the recipient of external funding to conduct research on nutritional supplements on the microbiome in athletes. MG reports no conflicts of interest regarding the material or paper presented. MG has previously received external funding to conduct research studies involving nutritional supplements including probiotics. DBP reports no conflicts of interest regarding the material or paper presented, and has received grants to evaluate the effectiveness of probiotic supplementation in athletes. BIC has conducted industry sponsored studies at his university and occasionally serves as a scientific and legal consultant related to exercise and nutrition intervention studies. He also serves on the scientific advisory board of Dymatize (Post Holdings). RBK reports no conflicts of interest related to the material presented in this paper. He has conducted industry sponsored studies at the universities he has been affiliated with and occasionally serves as a scientific and legal consultant related to exercise and nutrition intervention studies. CJW is employed by Jamieson Labs, a company selling branded probiotics products. MPA is employed by Biolab research Srl, performing research & development activities for Probiotical SpA, a leading probiotic supplier. DSK reports he works for a contract research organization that has received funding from the probiotic industry for clinical trials and serves on the Scientific Advisory Board for Dymatize (Post Holdings). JS is a co-founder of Fitbiomics, a company identifying, researching and commercializing new probiotic strains. JAT is employed by the International Probiotic Association and further consults within the probiotic and microbiome industries. PJA reports no conflicts of interest related to the material presented in this paper. He serves on the Scientific Advisory Board for Dymatize (Post Holdings), and Isagenix International LLC and has conducted industry sponsored studies involving nutritional supplements. SMA reports no conflicts of interest related to the material presented in this paper. He serves on the Scientific Advisory Board for Dymatize (Post Holdings) and has conducted industry sponsored studies involving nutritional supplements. JA is the CEO of the International Society of Sports Nutrition and reports no conflicts of interest with the material presented.

References

    1. Human Microbiome Project C Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214. doi: 10.1038/nature11234.
    1. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65. doi: 10.1038/nature08821.
    1. Cronin O, Molloy MG, Shanahan F. Exercise, fitness, and the gut. Curr Opin Gastroenterol. 2016;32(2):67–73. doi: 10.1097/MOG.0000000000000240.
    1. Ursell LK, Metcalf JL, Parfrey LW, Knight R. Defining the human microbiome. Nutr Rev. 2012;70(Suppl 1):S38–S44. doi: 10.1111/j.1753-4887.2012.00493.x.
    1. Duffy LC, Raiten DJ, Hubbard VS, Starke-Reed P. Progress and challenges in developing metabolic footprints from diet in human gut microbial cometabolism. J Nutr. 2015;145(5):1123S–1130S. doi: 10.3945/jn.114.194936.
    1. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–1697. doi: 10.1126/science.1177486.
    1. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–227. doi: 10.1038/nature11053.
    1. Dudek-Wicher RK, Junka A, Bartoszewicz M. The influence of antibiotics and dietary components on gut microbiota. Prz Gastroenterol. 2018;13(2):85–92.
    1. Flint HJ, Duncan SH, Scott KP, Louis P. Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc. 2015;74(1):13–22. doi: 10.1017/S0029665114001463.
    1. Wampach L, Heintz-Buschart A, Fritz JV, Ramiro-Garcia J, Habier J, Herold M, et al. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nat Commun. 2018;9(1):5091. doi: 10.1038/s41467-018-07631-x.
    1. Jang LG, Choi G, Kim SW, Kim BY, Lee S, Park H. The combination of sport and sport-specific diet is associated with characteristics of gut microbiota: an observational study. J Int Soc Sports Nutr. 2019;16(1):21. doi: 10.1186/s12970-019-0290-y.
    1. Bermon S, Petriz B, Kajeniene A, Prestes J, Castell L, Franco OL. The microbiota: an exercise immunology perspective. Exerc Immunol Rev. 2015;21:70–79.
    1. Barton W, Penney NC, Cronin O, Garcia-Perez I, Molloy MG, Holmes E, et al. The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level. Gut. 2018;67(4):625–633. doi: 10.1136/gutjnl-2016-313627.
    1. Estaki M, Pither J, Baumeister P, Little JP, Gill SK, Ghosh S, et al. Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. Microbiome. 2016;4(1):42. doi: 10.1186/s40168-016-0189-7.
    1. Clark A, Mach N. Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes. J Int Soc Sports Nutr. 2016;13:43. doi: 10.1186/s12970-016-0155-6.
    1. Scheiman J, Luber JM, Chavkin TA, MacDonald T, Tung A, Pham LD, et al. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med. 2019;25(7):1104–1109. doi: 10.1038/s41591-019-0485-4.
    1. Cerda B, Perez M, Perez-Santiago JD, Tornero-Aguilera JF, Gonzalez-Soltero R, Larrosa M. Gut microbiota modification: another piece in the puzzle of the benefits of physical exercise in health? Front Physiol. 2016;7:51. doi: 10.3389/fphys.2016.00051.
    1. Petersen LM, Bautista EJ, Nguyen H, Hanson BM, Chen L, Lek SH, et al. Community characteristics of the gut microbiomes of competitive cyclists. Microbiome. 2017;5(1):98. doi: 10.1186/s40168-017-0320-4.
    1. Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M, Hogan A, 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. Zhou Y, Mihindukulasuriya KA, Gao H, La Rosa PS, Wylie KM, Martin JC, et al. Exploration of bacterial community classes in major human habitats. Genome Biol. 2014;15(5):R66. doi: 10.1186/gb-2014-15-5-r66.
    1. O'Sullivan A, Farver M, Smilowitz JT. The influence of early infant-feeding practices on the intestinal microbiome and body composition in infants. Nutr Metab Insights. 2015;8(Suppl 1):1–9.
    1. Stein MM, Hrusch CL, Gozdz J, Igartua C, Pivniouk V, Murray SE, et al. Innate immunity and asthma risk in Amish and Hutterite farm children. N Engl J Med. 2016;375(5):411–421. doi: 10.1056/NEJMoa1508749.
    1. Zhang L, Nichols RG, Correll J, Murray IA, Tanaka N, Smith PB, et al. Persistent organic pollutants modify gut microbiota-host metabolic homeostasis in mice through aryl hydrocarbon receptor activation. Environ Health Perspect. 2015;123(7):679–688. doi: 10.1289/ehp.1409055.
    1. Fouhy F, Watkins C, Hill CJ, O'Shea CA, Nagle B, Dempsey EM, et al. Perinatal factors affect the gut microbiota up to four years after birth. Nat Commun. 2019;10(1):1517. doi: 10.1038/s41467-019-09252-4.
    1. Hollister EB, Riehle K, Luna RA, Weidler EM, Rubio-Gonzales M, Mistretta TA, et al. Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome. 2015;3:36. doi: 10.1186/s40168-015-0101-x.
    1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635–1638. doi: 10.1126/science.1110591.
    1. Wu HJ, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3(1):4–14. doi: 10.4161/gmic.19320.
    1. Harsch IA, Konturek PC. The Role of Gut Microbiota in Obesity and Type 2 and Type 1 Diabetes Mellitus: New Insights into "Old" Diseases. Med Sci (Basel). 2018;6(2) 10.3390/medsci6020032.
    1. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125(3):926–938. doi: 10.1172/JCI76304.
    1. Ishiguro E, Haskey N, Campbell K. Gut microbiota: interactive effects of nutrition and health: Elsevier. 2018.
    1. Tierney BT, Yang Z, Luber JM, Beaudin M, Wibowo MC, Baek C, et al. The landscape of genetic content in the gut and Oral human microbiome. Cell Host Microbe. 2019;26(2):283–95. e8. doi: 10.1016/j.chom.2019.07.008.
    1. Roager HM, Hansen LB, Bahl MI, Frandsen HL, Carvalho V, Gobel RJ, et al. Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut. Nat Microbiol. 2016;1(9):16093. doi: 10.1038/nmicrobiol.2016.93.
    1. Laureto L, Cianciaruso M, Samia D. Functional diversity: an overview of its history and applicability. Natureza & Conservacao. 2015;13(2):112–116. doi: 10.1016/j.ncon.2015.11.001.
    1. Backhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM, et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012;12(5):611–622. doi: 10.1016/j.chom.2012.10.012.
    1. Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med. 2016;8(1):51. doi: 10.1186/s13073-016-0307-y.
    1. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489(7415):220–230. doi: 10.1038/nature11550.
    1. Rodriguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N, et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015;26:26050.
    1. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, et al. The long-term stability of the human gut microbiota. Science. 2013;341(6141):1237439. doi: 10.1126/science.1237439.
    1. Visconti A, Le Roy CI, Rosa F, Rossi N, Martin TC, Mohney RP, et al. Interplay between the human gut microbiome and host metabolism. Nat Commun. 2019;10(1):4505. doi: 10.1038/s41467-019-12476-z.
    1. Heintz-Buschart A, Wilmes P. Human gut microbiome: function matters. Trends Microbiol. 2018;26(7):563–574. doi: 10.1016/j.tim.2017.11.002.
    1. Turnbaugh PJ, Gordon JI. An invitation to the marriage of metagenomics and metabolomics. Cell. 2008;134(5):708–713. doi: 10.1016/j.cell.2008.08.025.
    1. Allaband C, McDonald D, Vazquez-Baeza Y, Minich JJ, Tripathi A, Brenner DA, et al. Microbiome 101: studying, analyzing, and interpreting gut microbiome data for clinicians. Clin Gastroenterol Hepatol. 2019;17(2):218–230. doi: 10.1016/j.cgh.2018.09.017.
    1. Knight R, Callewaert C, Marotz C, Hyde ER, Debelius JW, McDonald D, et al. The microbiome and human biology. Annu Rev Genomics Hum Genet. 2017;18:65–86. doi: 10.1146/annurev-genom-083115-022438.
    1. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, et al. Conducting a microbiome study. Cell. 2014;158(2):250–262. doi: 10.1016/j.cell.2014.06.037.
    1. Poretsky R, Rodriguez RL, Luo C, Tsementzi D, Konstantinidis KT. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS One. 2014;9(4):e93827. doi: 10.1371/journal.pone.0093827.
    1. Janda JM, Abbott SL. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol. 2007;45(9):2761–2764. doi: 10.1128/JCM.01228-07.
    1. Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol. 2007;73(5):1576–1585. doi: 10.1128/AEM.01996-06.
    1. Vernocchi P, Del Chierico F, Putignani L. Gut microbiota profiling: metabolomics based approach to unravel compounds affecting human health. Front Microbiol. 2016;7:1144. doi: 10.3389/fmicb.2016.01144.
    1. Marcobal A, Kashyap PC, Nelson TA, Aronov PA, Donia MS, Spormann A, et al. A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice. ISME J. 2013;7(10):1933–1943. doi: 10.1038/ismej.2013.89.
    1. Zierer J, Jackson MA, Kastenmuller G, Mangino M, Long T, Telenti A, et al. The fecal metabolome as a functional readout of the gut microbiome. Nat Genet. 2018;50(6):790–795. doi: 10.1038/s41588-018-0135-7.
    1. Bisanz JE, Upadhyay V, Turnbaugh JA, Ly K, Turnbaugh PJ. Meta-analysis reveals reproducible gut microbiome alterations in response to a high-fat diet. Cell Host Microbe. 2019;26(2):265–72.e4. doi: 10.1016/j.chom.2019.06.013.
    1. Barb JJ, Oler AJ, Kim HS, Chalmers N, Wallen GR, Cashion A, et al. Development of an analysis pipeline characterizing multiple hypervariable regions of 16S rRNA using mock samples. PLoS One. 2016;11(2):e0148047. doi: 10.1371/journal.pone.0148047.
    1. Kemppainen KM, Ardissone AN, Davis-Richardson AG, Fagen JR, Gano KA, Leon-Novelo LG, et al. Early childhood gut microbiomes show strong geographic differences among subjects at high risk for type 1 diabetes. Diabetes Care. 2015;38(2):329–332. doi: 10.2337/dc14-0850.
    1. Lee S, Sung J, Lee J, Ko G. Comparison of the gut microbiotas of healthy adult twins living in South Korea and the United States. Appl Environ Microbiol. 2011;77(20):7433–7437. doi: 10.1128/AEM.05490-11.
    1. Liu Z, DeSantis TZ, Andersen GL, Knight R. Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequencers. Nucleic Acids Res. 2008;36(18):e120. doi: 10.1093/nar/gkn491.
    1. Bressa C, Bailen-Andrino M, Perez-Santiago J, Gonzalez-Soltero R, Perez M, Montalvo-Lominchar MG, et al. Differences in gut microbiota profile between women with active lifestyle and sedentary women. PLoS One. 2017;12(2):e0171352. doi: 10.1371/journal.pone.0171352.
    1. Morkl S, Lackner S, Muller W, Gorkiewicz G, Kashofer K, Oberascher A, et al. Gut microbiota and body composition in anorexia nervosa inpatients in comparison to athletes, overweight, obese, and normal weight controls. Int J Eat Disord. 2017;50(12):1421–1431. doi: 10.1002/eat.22801.
    1. O'Donovan CM, Madigan SM, Garcia-Perez I, Rankin A. O OS, Cotter PD. distinct microbiome composition and metabolome exists across subgroups of elite Irish athletes. J Sci Med Sport. 2020;23(1):63–68. doi: 10.1016/j.jsams.2019.08.290.
    1. Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut. 2016;65(3):426–436. doi: 10.1136/gutjnl-2014-308778.
    1. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289–306. doi: 10.4161/gmic.19897.
    1. Hamer HM, Jonkers DM, Bast A, Vanhoutvin SA, Fischer MA, Kodde A, et al. Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clin Nutr. 2009;28(1):88–93. doi: 10.1016/j.clnu.2008.11.002.
    1. Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary Fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–1345. doi: 10.1016/j.cell.2016.05.041.
    1. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214. doi: 10.1126/science.1241214.
    1. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–2340. doi: 10.1194/jlr.R036012.
    1. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110(22):9066–9071. doi: 10.1073/pnas.1219451110.
    1. Olson CA, Vuong HE, Yano JM, Liang QY, Nusbaum DJ, Hsiao EY. The gut microbiota mediates the anti-seizure effects of the ketogenic diet. Cell. 2018;174(2):497. doi: 10.1016/j.cell.2018.06.051.
    1. Maffetone PB, Laursen PB. Athletes: fit but unhealthy? Sports Med Open. 2015;2:24. doi: 10.1186/s40798-016-0048-x.
    1. Cox AJ, West NP, Cripps AW. Obesity, inflammation, and the gut microbiota. Lancet Diabetes Endocrinol. 2015;3(3):207–215. doi: 10.1016/S2213-8587(14)70134-2.
    1. Khan MJ, Gerasimidis K, Edwards CA, Shaikh MG. Role of gut microbiota in the Aetiology of obesity: proposed mechanisms and review of the literature. J Obes. 2016;2016:7353642. doi: 10.1155/2016/7353642.
    1. Lira FS, Rosa JC, Pimentel GD, Souza HA, Caperuto EC, Carnevali LC, Jr, et al. Endotoxin levels correlate positively with a sedentary lifestyle and negatively with highly trained subjects. Lipids Health Dis. 2010;9:82. doi: 10.1186/1476-511X-9-82.
    1. Cook MD, Allen JM, Pence BD, Wallig MA, Gaskins HR, White BA, et al. Exercise and gut immune function: evidence of alterations in colon immune cell homeostasis and microbiome characteristics with exercise training. Immunol Cell Biol. 2016;94(2):158–163. doi: 10.1038/icb.2015.108.
    1. Matsumoto M, Inoue R, Tsukahara T, Ushida K, Chiji H, Matsubara N, et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem. 2008;72(2):572–576. doi: 10.1271/bbb.70474.
    1. Choi JJ, Eum SY, Rampersaud E, Daunert S, Abreu MT, Toborek M. Exercise attenuates PCB-induced changes in the mouse gut microbiome. Environ Health Perspect. 2013;121(6):725–730. doi: 10.1289/ehp.1306534.
    1. Evans CC, LePard KJ, Kwak JW, Stancukas MC, Laskowski S, Dougherty J, 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):e92193. doi: 10.1371/journal.pone.0092193.
    1. Lambert JE, Myslicki JP, Bomhof MR, Belke DD, Shearer J, Reimer RA. Exercise training modifies gut microbiota in normal and diabetic mice. Appl Physiol Nutr Metab. 2015;40(7):749–752. doi: 10.1139/apnm-2014-0452.
    1. Mathur R, Barlow GM. Obesity and the microbiome. Expert Rev Gastroenterol Hepatol. 2015;9(8):1087–1099. doi: 10.1586/17474124.2015.1051029.
    1. Salonen A, de Vos WM, Palva A. Gastrointestinal microbiota in irritable bowel syndrome: present state and perspectives. Microbiology. 2010;156(Pt 11):3205–3215. doi: 10.1099/mic.0.043257-0.
    1. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010;5(2):e9085. doi: 10.1371/journal.pone.0009085.
    1. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–1023. doi: 10.1038/4441022a.
    1. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102(31):11070–11075. doi: 10.1073/pnas.0504978102.
    1. Kasai C, Sugimoto K, Moritani I, Tanaka J, Oya Y, Inoue H, et al. Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol. 2015;15:100. doi: 10.1186/s12876-015-0330-2.
    1. Koliada A, Syzenko G, Moseiko V, Budovska L, Puchkov K, Perederiy V, et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17(1):120. doi: 10.1186/s12866-017-1027-1.
    1. Walters WA, Xu Z, Knight R. Meta-analyses of human gut microbes associated with obesity and IBD. FEBS Lett. 2014;588(22):4223–4233. doi: 10.1016/j.febslet.2014.09.039.
    1. Finucane MM, Sharpton TJ, Laurent TJ, Pollard KS. A taxonomic signature of obesity in the microbiome? Getting to the guts of the matter. PLoS One. 2014;9(1):e84689. doi: 10.1371/journal.pone.0084689.
    1. Johnson EL, Heaver SL, Walters WA, Ley RE. Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes. J Mol Med (Berl) 2017;95(1):1–8. doi: 10.1007/s00109-016-1492-2.
    1. Petriz BA, Castro AP, Almeida JA, Gomes CP, Fernandes GR, Kruger RH, et al. Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats. BMC Genomics. 2014;15:511. doi: 10.1186/1471-2164-15-511.
    1. Queipo-Ortuno MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM, Cardona F, 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):e65465. doi: 10.1371/journal.pone.0065465.
    1. Campbell SC, Wisniewski PJ, Noji M, McGuinness LR, Haggblom MM, Lightfoot SA, et al. The effect of diet and exercise on intestinal integrity and microbial diversity in mice. PLoS One. 2016;11(3):e0150502. doi: 10.1371/journal.pone.0150502.
    1. Kang SS, Jeraldo PR, Kurti A, Miller ME, Cook MD, Whitlock K, et al. Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition. Mol Neurodegener. 2014;9:36. doi: 10.1186/1750-1326-9-36.
    1. Mika A, Van Treuren W, Gonzalez A, Herrera JJ, 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):e0125889. doi: 10.1371/journal.pone.0125889.
    1. Bocker U, Nebe T, Herweck F, Holt L, Panja A, Jobin C, et al. Butyrate modulates intestinal epithelial cell-mediated neutrophil migration. Clin Exp Immunol. 2003;131(1):53–60. doi: 10.1046/j.1365-2249.2003.02056.x.
    1. Monteiro R, Azevedo I. Chronic inflammation in obesity and the metabolic syndrome. Mediat Inflamm. 2010;2010. 10.1155/2010/289645.
    1. Durk RP, Castillo E, Marquez-Magana L, Grosicki GJ, Bolter ND, Lee CM, et al. Gut microbiota composition is related to cardiorespiratory fitness in healthy Young adults. Int J Sport Nutr Exerc Metab. 2019;29(3):249–253. doi: 10.1123/ijsnem.2018-0024.
    1. Yang Y, Shi Y, Wiklund P, Tan X, Wu N, Zhang X, et al. The association between cardiorespiratory fitness and gut microbiota composition in premenopausal women. Nutrients. 2017;9(8):792. doi: 10.3390/nu9080792.
    1. Clavel T, Lepage P, Charrier C. The family Coriobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes. Berlin: Springer; 2014.
    1. Rycroft AN, Garside LH. Actinobacillus species and their role in animal disease. Vet J. 2000;159(1):18–36. doi: 10.1053/tvjl.1999.0403.
    1. Ng SK, Hamilton IR. Carbon dioxide fixation by Veillonella parvula M 4 and its relation to propionic acid formation. Can J Microbiol. 1973;19(6):715–723. doi: 10.1139/m73-116.
    1. Allen JM, Mailing LJ, Niemiro GM, Moore R, Cook MD, White BA, et al. Exercise alters gut microbiota composition and function in lean and obese humans. Med Sci Sports Exerc. 2018;50(4):747–757. doi: 10.1249/MSS.0000000000001495.
    1. Keohane DM, Woods T, O'Connor P, Underwood S, Cronin O, Whiston R, et al. Four men in a boat: ultra-endurance exercise alters the gut microbiome. J Sci Med Sport. 2019;22(9):1059–1064. doi: 10.1016/j.jsams.2019.04.004.
    1. Hawley JA. Microbiota and muscle highway - two way traffic. Nat Rev Endocrinol. 2019;16(2):71–72. doi: 10.1038/s41574-019-0291-6.
    1. Taniguchi H, Tanisawa K, Sun X, Kubo T, Hoshino Y, Hosokawa M, et al. Effects of short-term endurance exercise on gut microbiota in elderly men. Phys Rep. 2018;6(23):e13935. doi: 10.14814/phy2.13935.
    1. Pluznick JL. Microbial short-chain fatty acids and blood pressure regulation. Curr Hypertens Rep. 2017;19(4):25. doi: 10.1007/s11906-017-0722-5.
    1. Morita E, Yokoyama H, Imai D, Takeda R, Ota A, Kawai E, et al. Aerobic exercise training with brisk walking increases intestinal Bacteroides in healthy elderly women. Nutrients. 2019;11(4):868. doi: 10.3390/nu11040868.
    1. Santacruz A, Collado MC, Garcia-Valdes L, Segura MT, Martin-Lagos JA, Anjos T, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr. 2010;104(1):83–92. doi: 10.1017/S0007114510000176.
    1. Abenavoli L, Scarpellini E, Colica C, Boccuto L, Salehi B, Sharifi-Rad J, et al. Gut microbiota and obesity: a role for probiotics. Nutrients. 2019;11(11):2690. doi: 10.3390/nu11112690.
    1. Liu Y, Wang Y, Ni Y, Cheung CKY, Lam KSL, Wang Y, et al. Gut Microbiome Fermentation Determines the Efficacy of Exercise for Diabetes Prevention. Cell Metab. 2019;31(1):P77–91.E5. doi: 10.1016/j.cmet.2019.11.001.
    1. Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF, et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009;9(4):311–326. doi: 10.1016/j.cmet.2009.02.002.
    1. Kern T, Blond MB, Hansen TH, Rosenkilde M, Quist JS, Gram AS, et al. Structured exercise alters the gut microbiota in humans with overweight and obesity-a randomized controlled trial. Int J Obes. 2019;44:125–135. doi: 10.1038/s41366-019-0440-y.
    1. Motiani KK, Collado MC, Eskelinen JJ, Virtanen KA, Loyttyniemi E, Salminen S, et al. Exercise training modulates gut microbiota profile and improves Endotoxemia. Med Sci Sports Exerc. 2019;52(1):94–104. doi: 10.1249/MSS.0000000000002112.
    1. Rajilic-Stojanovic M, de Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev. 2014;38(5):996–1047. doi: 10.1111/1574-6976.12075.
    1. Tuovinen E, Keto J, Nikkila J, Matto J, Lahteenmaki K. Cytokine response of human mononuclear cells induced by intestinal Clostridium species. Anaerobe. 2013;19:70–76. doi: 10.1016/j.anaerobe.2012.11.002.
    1. Ohtani M, Sugita M, Maruyama K. Amino acid mixture improves training efficiency in athletes. J Nutr. 2006;136(2):538S–543S. doi: 10.1093/jn/136.2.538S.
    1. Metges CC. Contribution of microbial amino acids to amino acid homeostasis of the host. J Nutr. 2000;130(7):1857S–1864S. doi: 10.1093/jn/130.7.1857S.
    1. Gisolfi CV. Is the GI system built for exercise? News Physiol Sci. 2000;15:114–119.
    1. Rosa EF, Silva AC, Ihara SS, Mora OA, Aboulafia J, Nouailhetas VL. Habitual exercise program protects murine intestinal, skeletal, and cardiac muscles against aging. J Appl Physiol. 2005;99(4):1569–1575. doi: 10.1152/japplphysiol.00417.2005.
    1. Tottey W, Feria-Gervasio D, Gaci N, Laillet B, Pujos E, Martin JF, et al. Colonic transit time is a driven force of the gut microbiota composition and metabolism: in vitro evidence. J Neurogastroenterol Motil. 2017;23(1):124–134. doi: 10.5056/jnm16042.
    1. Abbas A, Wilding G, Sitrin M. Does colonic transit time affect colonic pH? J Gastroenterol Hepatol Res. 2014;3(6):1103–1107. doi: 10.6051/j.issn.2224-3992.2014.03.399.
    1. Strid H, Simren M, Storsrud S, Stotzer PO, Sadik R. Effect of heavy exercise on gastrointestinal transit in endurance athletes. Scand J Gastroenterol. 2011;46(6):673–677. doi: 10.3109/00365521.2011.558110.
    1. De Schryver AM, Keulemans YC, Peters HP, Akkermans LM, Smout AJ, De Vries WR, et al. Effects of regular physical activity on defecation pattern in middle-aged patients complaining of chronic constipation. Scand J Gastroenterol. 2005;40(4):422–429. doi: 10.1080/00365520510011641.
    1. Oettle GJ. Effect of moderate exercise on bowel habit. Gut. 1991;32(8):941–944. doi: 10.1136/gut.32.8.941.
    1. Horner KM, Schubert MM, Desbrow B, Byrne NM, King NA. Acute exercise and gastric emptying: a meta-analysis and implications for appetite control. Sports Med. 2015;45(5):659–678. doi: 10.1007/s40279-014-0285-4.
    1. Rehrer NJ, Beckers E, Brouns F, Hoor ten F, Saris WH. Exercise and training effects on gastric emptying of carbohydrate beverages. Med Sci Sports Exerc. 1989;21(5):540–549. doi: 10.1249/00005768-198910000-00008.
    1. Neufer PD, Young AJ, Sawka MN. Gastric emptying during walking and running: effects of varied exercise intensity. Eur J Appl Physiol Occup Physiol. 1989;58(4):440–445. doi: 10.1007/BF00643522.
    1. Feldman M, Nixon JV. Effect of exercise on postprandial gastric secretion and emptying in humans. J Appl Physiol Respir Environ Exerc Physiol. 1982;53(4):851–854.
    1. Walker AW, Duncan SH, McWilliam Leitch EC, Child MW, Flint HJ. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol. 2005;71(7):3692–3700. doi: 10.1128/AEM.71.7.3692-3700.2005.
    1. Qamar MI, Read AE. Effects of exercise on mesenteric blood flow in man. Gut. 1987;28(5):583–587. doi: 10.1136/gut.28.5.583.
    1. de Oliveira EP, Burini RC. The impact of physical exercise on the gastrointestinal tract. Curr Opin Clin Nutr Metab Care. 2009;12(5):533–538. doi: 10.1097/MCO.0b013e32832e6776.
    1. Oktedalen O, Lunde OC, Opstad PK, Aabakken L, Kvernebo K. Changes in the gastrointestinal mucosa after long-distance running. Scand J Gastroenterol. 1992;27(4):270–274. doi: 10.3109/00365529209000073.
    1. Zuhl M, Schneider S, Lanphere K, Conn C, Dokladny K, Moseley P. Exercise regulation of intestinal tight junction proteins. Br J Sports Med. 2014;48(12):980–986. doi: 10.1136/bjsports-2012-091585.
    1. Brock-Utne JG, Gaffin SL, Wells MT, Gathiram P, Sohar E, James MF, et al. Endotoxaemia in exhausted runners after a long-distance race. S Afr Med J. 1988;73(9):533–536.
    1. Luo B, Xiang D, Nieman DC, Chen P. The effects of moderate exercise on chronic stress-induced intestinal barrier dysfunction and antimicrobial defense. Brain Behav Immun. 2014;39:99–106. doi: 10.1016/j.bbi.2013.11.013.
    1. Johannesson E, Simren M, Strid H, Bajor A, Sadik R. Physical activity improves symptoms in irritable bowel syndrome: a randomized controlled trial. Am J Gastroenterol. 2011;106(5):915–922. doi: 10.1038/ajg.2010.480.
    1. Cronin O, O'Sullivan O, Barton W, Cotter PD, Molloy MG, Shanahan F. Gut microbiota: implications for sports and exercise medicine. Br J Sports Med. 2017;51(9):700–701. doi: 10.1136/bjsports-2016-097225.
    1. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. doi: 10.1038/nature12820.
    1. Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, et al. Population-level analysis of gut microbiome variation. Science. 2016;352(6285):560–564. doi: 10.1126/science.aad3503.
    1. Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016;352(6285):565–569. doi: 10.1126/science.aad3369.
    1. Portune K, Beaumont M, Davila A, Tome D, Blachier F, Sanz Y. Gut microbiota role in dietary protein metabolism and health-related outcomes: the two sides of the coin. Trends Food Sci Technol. 2016;57:213–232. doi: 10.1016/j.tifs.2016.08.011.
    1. Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, et al. Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr. 2018;57(1):1–24. doi: 10.1007/s00394-017-1445-8.
    1. Neis EP, Dejong CH, Rensen SS. The role of microbial amino acid metabolism in host metabolism. Nutrients. 2015;7(4):2930–2946. doi: 10.3390/nu7042930.
    1. Kerksick CM, Wilborn CD, Roberts MD, Smith-Ryan A, Kleiner SM, Jager R, et al. ISSN exercise & sports nutrition review update: research & recommendations. J Int Soc Sports Nutr. 2018;15(1):38. doi: 10.1186/s12970-018-0242-y.
    1. Tiller NB, Roberts JD, Beasley L, Chapman S, Pinto JM, Smith L, et al. International Society of Sports Nutrition Position Stand: nutritional considerations for single-stage ultra-marathon training and racing. J Int Soc Sports Nutr. 2019;16(1):50. doi: 10.1186/s12970-019-0312-9.
    1. Krajmalnik-Brown R, Ilhan ZE, Kang DW, DiBaise JK. Effects of gut microbes on nutrient absorption and energy regulation. Nutr Clin Pract. 2012;27(2):201–214. doi: 10.1177/0884533611436116.
    1. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70(2):567–590. doi: 10.1152/physrev.1990.70.2.567.
    1. Parker DS. The measurement of production rates of volatile fatty acids in the caecum of the conscious rabbit. Br J Nutr. 1976;36(1):61–70. doi: 10.1079/BJN19760058.
    1. Rosenbaum M, Knight R, Leibel RL. The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol Metab. 2015;26(9):493–501. doi: 10.1016/j.tem.2015.07.002.
    1. Heiss CN, Olofsson LE. Gut microbiota-dependent modulation of energy metabolism. J Innate Immun. 2018;10(3):163–171. doi: 10.1159/000481519.
    1. Donia MS, Fischbach MA. Small molecules from the human microbiota. Science. 2015;349(6246):1254766. doi: 10.1126/science.1254766.
    1. Riedl RA, Atkinson SN, Burnett CML, Grobe JL, Kirby JR. The gut microbiome, energy homeostasis, and implications for hypertension. Curr Hypertens Rep. 2017;19(4):27. doi: 10.1007/s11906-017-0721-6.
    1. Avolio E, Gualtieri P, Romano L, Pecorella C, Ferraro S, Di Renzo L, et al. Obesity and body composition in man and woman: associated diseases and new role of gut microbiota. Curr Med Chem. 2019;27(2):216–229. doi: 10.2174/0929867326666190326113607.
    1. Tagliabue A, Elli M. The role of gut microbiota in human obesity: recent findings and future perspectives. Nutr Metab Cardiovasc Dis. 2013;23(3):160–168. doi: 10.1016/j.numecd.2012.09.002.
    1. Scheithauer TP, Dallinga-Thie GM, de Vos WM, Nieuwdorp M, van Raalte DH. Causality of small and large intestinal microbiota in weight regulation and insulin resistance. Mol Metab. 2016;5(9):759–770. doi: 10.1016/j.molmet.2016.06.002.
    1. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–1031. doi: 10.1038/nature05414.
    1. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101(44):15718–15723. doi: 10.1073/pnas.0407076101.
    1. Vaughn AC, Cooper EM, DiLorenzo PM, O'Loughlin LJ, Konkel ME, Peters JH, et al. Energy-dense diet triggers changes in gut microbiota, reorganization of gutbrain vagal communication and increases body fat accumulation. Acta Neurobiol Exp. 2017;77(1):18–30.
    1. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–484. doi: 10.1038/nature07540.
    1. Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N, Le Chatelier E, et al. Dietary intervention impact on gut microbial gene richness. Nature. 2013;500(7464):585–588. doi: 10.1038/nature12480.
    1. Jumpertz R, Le DS, Turnbaugh PJ, Trinidad C, Bogardus C, Gordon JI, et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr. 2011;94(1):58–65. doi: 10.3945/ajcn.110.010132.
    1. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, et al. The IOC consensus statement: beyond the female athlete triad--relative energy deficiency in sport (RED-S) Br J Sports Med. 2014;48(7):491–497. doi: 10.1136/bjsports-2014-093502.
    1. Zheng X, Wang S, Jia W. Calorie restriction and its impact on gut microbial composition and global metabolism. Front Med. 2018;12(6):634–644. doi: 10.1007/s11684-018-0670-8.
    1. Tanca A, Abbondio M, Palomba A, Fraumene C, Marongiu F, Serra M, et al. Caloric restriction promotes functional changes involving short-chain fatty acid biosynthesis in the rat gut microbiota. Sci Rep. 2018;8(1):14778. doi: 10.1038/s41598-018-33100-y.
    1. Aron-Wisnewsky J, Dore J, Clement K. The importance of the gut microbiota after bariatric surgery. Nat Rev Gastroenterol Hepatol. 2012;9(10):590–598. doi: 10.1038/nrgastro.2012.161.
    1. Rejeh N, Ahmadi F, Mohammadi E, Anoosheh M, Kazemnejad A. Barriers to, and facilitators of post-operative pain management in Iranian nursing: a qualitative research study. Int Nurs Rev. 2008;55(4):468–475. doi: 10.1111/j.1466-7657.2008.00659.x.
    1. Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010;59(12):3049–3057. doi: 10.2337/db10-0253.
    1. Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016;351(6275) 10.1126/science.aad3311.
    1. Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–421. doi: 10.1038/nature13421.
    1. Charbonneau MR, O'Donnell D, Blanton LV, Totten SM, Davis JC, Barratt MJ, et al. Sialylated Milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell. 2016;164(5):859–871. doi: 10.1016/j.cell.2016.01.024.
    1. Mack I, Penders J, Cook J, Dugmore J, Mazurak N, Enck P. Is the impact of starvation on the gut microbiota specific or unspecific to anorexia nervosa? A narrative review based on a systematic literature search. Curr Neuropharmacol. 2018;16(8):1131–1149. doi: 10.2174/1570159X16666180118101354.
    1. Borgo F, Riva A, Benetti A, Casiraghi MC, Bertelli S, Garbossa S, et al. Microbiota in anorexia nervosa: the triangle between bacterial species, metabolites and psychological tests. PLoS One. 2017;12(6):e0179739. doi: 10.1371/journal.pone.0179739.
    1. Mack I, Cuntz U, Gramer C, Niedermaier S, Pohl C, Schwiertz A, et al. Weight gain in anorexia nervosa does not ameliorate the faecal microbiota, branched chain fatty acid profiles, and gastrointestinal complaints. Sci Rep. 2016;6:26752. doi: 10.1038/srep26752.
    1. Kleiman SC, Watson HJ, Bulik-Sullivan EC, Huh EY, Tarantino LM, Bulik CM, et al. The intestinal microbiota in acute anorexia nervosa and during Renourishment: relationship to depression, anxiety, and eating disorder psychopathology. Psychosom Med. 2015;77(9):969–981. doi: 10.1097/PSY.0000000000000247.
    1. Sheflin AM, Melby CL, Carbonero F, Weir TL. Linking dietary patterns with gut microbial composition and function. Gut Microbes. 2017;8(2):113–129. doi: 10.1080/19490976.2016.1270809.
    1. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–108. doi: 10.1126/science.1208344.
    1. Brinkworth GD, Noakes M, Clifton PM, Bird AR. Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations. Br J Nutr. 2009;101(10):1493–1502. doi: 10.1017/S0007114508094658.
    1. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol. 2007;73(4):1073–1078. doi: 10.1128/AEM.02340-06.
    1. Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr. 2011;93(5):1062–1072. doi: 10.3945/ajcn.110.002188.
    1. Magee EA, Richardson CJ, Hughes R, Cummings JH. Contribution of dietary protein to sulfide production in the large intestine: an in vitro and a controlled feeding study in humans. Am J Clin Nutr. 2000;72(6):1488–1494. doi: 10.1093/ajcn/72.6.1488.
    1. Rowan FE, Docherty NG, Coffey JC, O'Connell PR. Sulphate-reducing bacteria and hydrogen sulphide in the aetiology of ulcerative colitis. Br J Surg. 2009;96(2):151–158. doi: 10.1002/bjs.6454.
    1. Ma N, Tian Y, Wu Y, Ma X. Contributions of the interaction between dietary protein and gut microbiota to intestinal health. Curr Protein Pept Sci. 2017;18(8):795–808. doi: 10.2174/1389203718666170216153505.
    1. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180. doi: 10.1038/nature09944.
    1. Costea PI, Hildebrand F, Arumugam M, Backhed F, Blaser MJ, Bushman FD, et al. Enterotypes in the landscape of gut microbial community composition. Nat Microbiol. 2018;3(1):8–16. doi: 10.1038/s41564-017-0072-8.
    1. Knights D, Ward TL, McKinlay CE, Miller H, Gonzalez A, McDonald D, et al. Rethinking "enterotypes". Cell Host Microbe. 2014;16(4):433–437. doi: 10.1016/j.chom.2014.09.013.
    1. Macfarlane GT, Macfarlane S. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int. 2012;95(1):50–60. doi: 10.5740/jaoacint.SGE_Macfarlane.
    1. Rist VT, Weiss E, Eklund M, Mosenthin R. Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review. Animal. 2013;7(7):1067–1078. doi: 10.1017/S1751731113000062.
    1. McAllan L, Skuse P, Cotter PD, O'Connor P, Cryan JF, Ross RP, et al. Protein quality and the protein to carbohydrate ratio within a high fat diet influences energy balance and the gut microbiota in C57BL/6J mice. PLoS One. 2014;9(2):e88904. doi: 10.1371/journal.pone.0088904.
    1. Tranberg B, Hellgren LI, Lykkesfeldt J, Sejrsen K, Jeamet A, Rune I, et al. Whey protein reduces early life weight gain in mice fed a high-fat diet. PLoS One. 2013;8(8):e71439. doi: 10.1371/journal.pone.0071439.
    1. Belobrajdic DP, McIntosh GH, Owens JA. A high-whey-protein diet reduces body weight gain and alters insulin sensitivity relative to red meat in wistar rats. J Nutr. 2004;134(6):1454–1458. doi: 10.1093/jn/134.6.1454.
    1. Tipton KD, Wolfe RR. Protein and amino acids for athletes. J Sports Sci. 2004;22(1):65–79. doi: 10.1080/0264041031000140554.
    1. Jalanka-Tuovinen J, Salonen A, Nikkila J, Immonen O, Kekkonen R, Lahti L, et al. Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS One. 2011;6(7):e23035. doi: 10.1371/journal.pone.0023035.
    1. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104(34):13780–13785. doi: 10.1073/pnas.0706625104.
    1. Fujimoto T, Imaeda H, Takahashi K, Kasumi E, Bamba S, Fujiyama Y, et al. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn's disease. J Gastroenterol Hepatol. 2013;28(4):613–619. doi: 10.1111/jgh.12073.
    1. Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK. Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol. 2011;19(7):349–359. doi: 10.1016/j.tim.2011.05.006.
    1. Negro M, Giardina S, Marzani B, Marzatico F. Branched-chain amino acid supplementation does not enhance athletic performance but affects muscle recovery and the immune system. J Sports Med Phys Fitness. 2008;48(3):347–351.
    1. van Hall G, Raaymakers JS, Saris WH, Wagenmakers AJ. Ingestion of branched-chain amino acids and tryptophan during sustained exercise in man: failure to affect performance. J Physiol. 1995;486(Pt 3):789–794. doi: 10.1113/jphysiol.1995.sp020854.
    1. Newsholme EA, Blomstrand E. Branched-chain amino acids and central fatigue. J Nutr. 2006;136(1 Suppl):274S–276S. doi: 10.1093/jn/136.1.274S.
    1. Greer BK, Woodard JL, White JP, Arguello EM, Haymes EM. Branched-chain amino acid supplementation and indicators of muscle damage after endurance exercise. Int J Sport Nutr Exerc Metab. 2007;17(6):595–607. doi: 10.1123/ijsnem.17.6.595.
    1. Moreno-Perez D, Bressa C, Bailen M, Hamed-Bousdar S, Naclerio F, Carmona M, et al. Effect of a protein supplement on the gut microbiota of endurance athletes: a randomized, controlled. Double-Blind Pilot Study Nutrients. 2018;10(3):337.
    1. Williams BA, Zhang D, Lisle AT, Mikkelsen D, McSweeney CS, Kang S, et al. Soluble arabinoxylan enhances large intestinal microbial health biomarkers in pigs fed a red meat-containing diet. Nutrition. 2016;32(4):491–497. doi: 10.1016/j.nut.2015.10.008.
    1. Jager R, Shields KA, Lowery RP, De Souza EO, Partl JM, Hollmer C, et al. Probiotic Bacillus coagulans GBI-30, 6086 reduces exercise-induced muscle damage and increases recovery. PeerJ. 2016;4:e2276. doi: 10.7717/peerj.2276.
    1. Cronin O, Barton W, Skuse P, Penney NC, Garcia-Perez I, Murphy EF, et al. A Prospective Metagenomic and Metabolomic Analysis of the Impact of Exercise and/or Whey Protein Supplementation on the Gut Microbiome of Sedentary Adults. mSystems. 2018;3(3) 10.1128/mSystems.00044-18.
    1. Mukhopadhya I, Segal JP, Carding SR, Hart AL, Hold GL. The gut virome: the 'missing link' between gut bacteria and host immunity? Ther Adv Gastroenterol. 2019;12:1756284819836620. doi: 10.1177/1756284819836620.
    1. Butteiger DN, Hibberd AA, McGraw NJ, Napawan N, Hall-Porter JM, Krul ES. Soy protein compared with Milk protein in a Western diet increases gut microbial diversity and reduces serum lipids in Golden Syrian hamsters. J Nutr. 2016;146(4):697–705. doi: 10.3945/jn.115.224196.
    1. Gentile CL, Ward E, Holst JJ, Astrup A, Ormsbee MJ, Connelly S, et al. Resistant starch and protein intake enhances fat oxidation and feelings of fullness in lean and overweight/obese women. Nutr J. 2015;14:113. doi: 10.1186/s12937-015-0104-2.
    1. Martens EC. Microbiome: fibre for the future. Nature. 2016;529(7585):158–159. doi: 10.1038/529158a.
    1. El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol. 2013;11(7):497–504. doi: 10.1038/nrmicro3050.
    1. Simpson HL, Campbell BJ. Review article: dietary fibre-microbiota interactions. Aliment Pharmacol Ther. 2015;42(2):158–179. doi: 10.1111/apt.13248.
    1. Tap J, Furet JP, Bensaada M, Philippe C, Roth H, Rabot S, et al. Gut microbiota richness promotes its stability upon increased dietary fibre intake in healthy adults. Environ Microbiol. 2015;17(12):4954–4964. doi: 10.1111/1462-2920.13006.
    1. O'Keefe SJ, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015;6:6342. doi: 10.1038/ncomms7342.
    1. Cramp T, Broad E, Martin D, Meyer BJ. Effects of preexercise carbohydrate ingestion on mountain bike performance. Med Sci Sports Exerc. 2004;36(9):1602–1609. doi: 10.1249/01.MSS.0000139805.91675.5B.
    1. Jacobs KA, Sherman WM. The efficacy of carbohydrate supplementation and chronic high- carbohydrate diets for improving endurance performance. Int J Sport Nutr. 1999;9(1):92–115. doi: 10.1123/ijsn.9.1.92.
    1. Gorvitovskaia A, Holmes SP, Huse SM. Interpreting Prevotella and Bacteroides as biomarkers of diet and lifestyle. Microbiome. 2016;4:15. doi: 10.1186/s40168-016-0160-7.
    1. Lim MY, Rho M, Song YM, Lee K, Sung J, Ko G. Stability of gut enterotypes in Korean monozygotic twins and their association with biomarkers and diet. Sci Rep. 2014;4:7348. doi: 10.1038/srep07348.
    1. Nakayama J, Watanabe K, Jiang J, Matsuda K, Chao SH, Haryono P, et al. Diversity in gut bacterial community of school-age children in Asia. Sci Rep. 2015;5:8397. doi: 10.1038/srep08397.
    1. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107(33):14691–14696. doi: 10.1073/pnas.1005963107.
    1. Liu Y, Zhang L, Wang X, Wang Z, Zhang J, Jiang R, et al. Similar fecal microbiota signatures in patients with diarrhea-predominant irritable bowel syndrome and patients with depression. Clin Gastroenterol Hepatol. 2016;14(11):1602–11.e5. doi: 10.1016/j.cgh.2016.05.033.
    1. Moreno-Indias I, Sanchez-Alcoholado L, Garcia-Fuentes E, Cardona F, Queipo-Ortuno MI, Tinahones FJ. Insulin resistance is associated with specific gut microbiota in appendix samples from morbidly obese patients. Am J Transl Res. 2016;8(12):5672–5684.
    1. Michail S, Lin M, Frey MR, Fanter R, Paliy O, Hilbush B, et al. Altered gut microbial energy and metabolism in children with non-alcoholic fatty liver disease. FEMS Microbiol Ecol. 2015;91(2):1–9. doi: 10.1093/femsec/fiu002.
    1. Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G, et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5(1):14. doi: 10.1186/s40168-016-0222-x.
    1. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One. 2012;7(6):e39743. doi: 10.1371/journal.pone.0039743.
    1. Precup G, Vodnar DC. Gut Prevotella as a possible biomarker of diet and its eubiotic versus dysbiotic roles: a comprehensive literature review. Br J Nutr. 2019;122(2):131–140. doi: 10.1017/S0007114519000680.
    1. Thomas DT, Erdman KA, Burke LM. American College of Sports Medicine joint position statement. Nutrition and athletic performance. Med Sci Sports Exerc. 2016;48(3):543–568. doi: 10.1249/MSS.0000000000000852.
    1. Jeukendrup AE. Training the gut for athletes. Sports Med. 2017;47(Suppl 1):101–110. doi: 10.1007/s40279-017-0690-6.
    1. Toden S, Bird AR, Topping DL, Conlon MA. Resistant starch prevents colonic DNA damage induced by high dietary cooked red meat or casein in rats. Cancer Biol Ther. 2006;5(3):267–272. doi: 10.4161/cbt.5.3.2382.
    1. Samuel BS, Hansen EE, Manchester JK, Coutinho PM, Henrissat B, Fulton R, et al. Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc Natl Acad Sci U S A. 2007;104(25):10643–10648. doi: 10.1073/pnas.0704189104.
    1. Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11(10):577–591. doi: 10.1038/nrendo.2015.128.
    1. Roelofsen H, Priebe MG, Vonk RJ. The interaction of short-chain fatty acids with adipose tissue: relevance for prevention of type 2 diabetes. Benefic Microbes. 2010;1(4):433–437. doi: 10.3920/BM2010.0028.
    1. Kaji I, Karaki S, Kuwahara A. Short-chain fatty acid receptor and its contribution to glucagon-like peptide-1 release. Digestion. 2014;89(1):31–36. doi: 10.1159/000356211.
    1. Astbury SM, Corfe BM. Uptake and metabolism of the short-chain fatty acid butyrate, a critical review of the literature. Curr Drug Metab. 2012;13(6):815–821. doi: 10.2174/138920012800840428.
    1. den Besten G, Bleeker A, Gerding A, van Eunen K, Havinga R, van Dijk TH, et al. Short-chain fatty acids protect against high-fat diet-induced obesity via a PPARgamma-dependent switch from lipogenesis to fat oxidation. Diabetes. 2015;64(7):2398–2408. doi: 10.2337/db14-1213.
    1. Caesar R, Tremaroli V, Kovatcheva-Datchary P, Cani PD, Backhed F. Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab. 2015;22(4):658–668. doi: 10.1016/j.cmet.2015.07.026.
    1. Murtaza N, Burke LM, Vlahovich N, Charlesson B, H ON, Ross ML, et al. The Effects of Dietary Pattern during Intensified Training on Stool Microbiota of Elite Race Walkers. Nutrients. 2019;11(2) 10.3390/nu11020261.
    1. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105(43):16731–16736. doi: 10.1073/pnas.0804812105.
    1. Fiorucci S, Distrutti E. Bile acid-activated receptors, intestinal microbiota, and the treatment of metabolic disorders. Trends Mol Med. 2015;21(11):702–714. doi: 10.1016/j.molmed.2015.09.001.
    1. Lopez-Siles M, Khan TM, Duncan SH, Harmsen HJ, Garcia-Gil LJ, Flint HJ. Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol. 2012;78(2):420–428. doi: 10.1128/AEM.06858-11.
    1. Burke LM, Hawley JA, Jeukendrup A, Morton JP, Stellingwerff T, Maughan RJ. Toward a common understanding of diet-exercise strategies to manipulate fuel availability for training and competition preparation in endurance sport. Int J Sport Nutr Exerc Metab. 2018;28(5):451–463. doi: 10.1123/ijsnem.2018-0289.
    1. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79(17):5112–5120. doi: 10.1128/AEM.01043-13.
    1. Revicki DA, Wood M, Wiklund I, Crawley J. Reliability and validity of the gastrointestinal symptom rating scale in patients with gastroesophageal reflux disease. Qual Life Res. 1998;7(1):75–83. doi: 10.1023/A:1008841022998.
    1. Blake MR, Raker JM, Whelan K. Validity and reliability of the Bristol stool form scale in healthy adults and patients with diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther. 2016;44(7):693–703. doi: 10.1111/apt.13746.
    1. Cardona S, Eck A, Cassellas M, Gallart M, Alastrue C, Dore J, et al. Storage conditions of intestinal microbiota matter in metagenomic analysis. BMC Microbiol. 2012;12:158. doi: 10.1186/1471-2180-12-158.
    1. Roesch LF, Casella G, Simell O, Krischer J, Wasserfall CH, Schatz D, et al. Influence of fecal sample storage on bacterial community diversity. Open Microbiol J. 2009;3:40–46. doi: 10.2174/1874285800903010040.
    1. Li F, Hullar MA, Lampe JW. Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J Microbiol Methods. 2007;68(2):303–311. doi: 10.1016/j.mimet.2006.09.006.
    1. Debelius J, Song SJ, Vazquez-Baeza Y, Xu ZZ, Gonzalez A, Knight R. Tiny microbes, enormous impacts: what matters in gut microbiome studies? Genome Biol. 2016;17(1):217. doi: 10.1186/s13059-016-1086-x.
    1. Liang Y, Dong T, Chen M, He L, Wang T, Liu X, et al. Systematic Analysis of Impact of Sampling Regions and Storage Methods on Fecal Gut Microbiome and Metabolome Profiles. mSphere. 2020;5(1) 10.1128/mSphere.00763-19.

Source: PubMed

3
Subscribe