Effects of short-term endurance exercise on gut microbiota in elderly men

Hirokazu Taniguchi, Kumpei Tanisawa, Xiaomin Sun, Takafumi Kubo, Yuri Hoshino, Masahito Hosokawa, Haruko Takeyama, Mitsuru Higuchi, Hirokazu Taniguchi, Kumpei Tanisawa, Xiaomin Sun, Takafumi Kubo, Yuri Hoshino, Masahito Hosokawa, Haruko Takeyama, Mitsuru Higuchi

Abstract

Regular exercise reduces the risks for cardiovascular diseases. Although the gut microbiota has been associated with fitness level and cardiometabolic risk factors, the effects of exercise-induced gut microbiota changes in elderly individuals are unclear. This study evaluated whether endurance exercise modulates the gut microbiota in elderly subjects, and whether these changes are associated with host cardiometabolic phenotypes. In a randomized crossover trial, 33 elderly Japanese men participated in a 5-week endurance exercise program. 16S rRNA gene-based metagenomic analyses revealed that the effect of endurance exercise on gut microbiota diversity was not greater than interindividual differences, whereas changes in α-diversity indices during intervention were negatively correlated with changes in systolic and diastolic blood pressure, especially during exercise. Microbial composition analyses showed that the relative abundance of Clostridium difficile significantly decreased, whereas that of Oscillospira significantly increased during exercise as compared to the control period. The changes in these taxa were correlated with the changes in several cardiometabolic risk factors. The findings indicate that short-term endurance exercise has little effect on gut microbiota in elderly individuals, and that the changes in gut microbiota were associated with cardiometabolic risk factors, such as systolic and diastolic blood pressure, providing preliminary insight into the associations between the gut microbiota and cardiometabolic phenotypes.

Keywords: Clostridium difficile; Oscillospira; Cardiovascular health; PICRUSt; microbiome.

© 2018 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of The Physiological Society and the American Physiological Society.

Figures

Figure 1
Figure 1
Flow diagram of the randomized crossover trial.
Figure 2
Figure 2
Gut microbial communities during exercise and control periods. Images represent individual principal coordinate analysis plots showing gut microbial communities at the operational taxonomic unit level before and after the exercise intervention based on (A and D) unweighted UniFrac distance, (B and E) weighted UniFrac distance, and (C and F) Bray‐Curtis dissimilarity matrices. In the upper figures (A–C), same colors on plots indicate the same individual before and after exercise. In the lower figures (D–F), blue plots represent individuals before exercise and red plots represent individuals after exercise.
Figure 3
Figure 3
Association between changes in α‐diversity indices and changes in brachial blood pressure during intervention. Associations between (A) Shannon index and SBP, (B) observed OTUs and SBP, (C) Shannon index and DBP, (D) observed OTUs and DBP. Open circles represent changes in values during the exercise period; closed circles represent changes in values during control periods. Correlation was evaluated by Spearman's rank correlation coefficients. The level of statistical significance was set at P < 0.05.
Figure 4
Figure 4
Comparison of changes in the relative abundance of (A) Oscillospira and (B) Clostridium difficile between exercise and control periods. Changes in the relative abundance of Oscillospira and C. difficile are presented as box‐plots with the median value and interquartile range. Significant differences were evaluated by the Mann–Whitney U test. The level of statistical significance was set at P < 0.05.
Figure 5
Figure 5
Changes in predicted metagenome functions that were significantly different between control and exercise periods. Changes in the relative abundance of each metagenomic function predicted based on the KEGG database are presented as box‐plots with the median value and the interquartile range. Significant differences were evaluated by the Mann–Whitney U test. All of the changes in metagenomic functions were significantly different between the exercise and control periods at the significance level of 0.05 and FDR < 0.3.

References

    1. Adnan, S. , Nelson J. W., Ajami N. J., Venna V. R., Petrosino J. F., Bryan R. M. Jr, et al. 2017. Alterations in the gut microbiota can elicit hypertension in rats. Physiol. Genomics 49:96–104.
    1. Allen, J. M. , Mailing L. J., Niemiro G. M., Moore R., Cook M. D., White B. A., et al. 2018. Exercise alters gut microbiota composition and function in lean and obese humans. Med. Sci. Sports Exerc. 50:747–757.
    1. Bishara, J. , Farah R., Mograbi J., Khalaila W., Abu‐Elheja O., Mahamid M., et al. 2013. Obesity as a risk factor for Clostridium difficile infection. Clin. Infect. Dis. 57:489–493.
    1. Bolger, A. M. , Lohse M., and Usadel B.. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.
    1. Bouchard, C. , Blair S. N., Church T. S., Earnest C. P., Hagberg J. M., Hakkinen K., et al. 2012. Adverse metabolic response to regular exercise: is it a rare or common occurrence? PLoS ONE 7:e37887.
    1. Bray, J. R. , and Curtis J. T.. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27:325–349.
    1. Burke, K. E. , and Lamont J. T.. 2014. Clostridium difficile infection: a worldwide disease. Gut. Liv. 8:1–6.
    1. Caporaso, J. G. , Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. 2010. QIIME allows analysis of high‐throughput community sequencing data. Nat. Methods 7:335–336.
    1. Chen, J. , He X., and Huang J.. 2014. Diet effects in gut microbiome and obesity. J. Food Sci. 79:R442–R451.
    1. Claesson, M. J. , Jeffery I. B., Conde S., Power S. E., O'Connor E. M., Cusack S., et al. 2012. Gut microbiota composition correlates with diet and health in the elderly. Nature 488:178–184.
    1. Clarke, S. F. , Murphy E. F., O'Sullivan O., Lucey A. J., Humphreys M., Hogan A., et al. 2014. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63:1913–1920.
    1. Collins, D. A. , Hawkey P. M., and Riley T. V.. 2013. Epidemiology of Clostridium difficile infection in Asia. Antimicrob. Resist. Infect. Control 2:21.
    1. Cornelissen, V. A. , and Fagard R. H.. 2005. Effects of endurance training on blood pressure, blood pressure‐regulating mechanisms, and cardiovascular risk factors. Hypertension 46:667–675.
    1. Costello, E. K. , Lauber C. L., Hamady M., Fierer N., Gordon J. I., and Knight R.. 2009. Bacterial community variation in human body habitats across space and time. Science 326:1694–1697.
    1. Denou, E. , Marcinko K., Surette M. G., Steinberg G. R., and Schertzer J. D.. 2016. High‐intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet‐induced obesity. Am. J. Physiol. Endocrinol. Metab. 310:E982–E993.
    1. Edgar, R. C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.
    1. Estaki, M. , Pither J., Baumeister P., Little J. P., Gill S. K., Ghosh S., et al. 2016. Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. Microbiome 4:42.
    1. Evans, C. C. , LePard K. J., Kwak J. W., Stancukas M. C., Laskowski S., Dougherty J., et al. 2014. Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet‐induced obesity. PLoS ONE 9:e92193.
    1. Garber, C. E. , Blissmer B., Deschenes M. R., Franklin B. A., Lamonte M. J., Lee I. M., et al. ; American College of Sports M, American College of Sports Medicine position stand . 2011. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med. Sci. Sports Exerc. 43: 1334–1359.
    1. Goodrich, J. K. , Waters J. L., Poole A. C., Sutter J. L., Koren O., Blekhman R., et al. 2014. Human genetics shape the gut microbiome. Cell 159:789–799.
    1. Hisada, T. , Endoh K., and Kuriki K.. 2015. Inter‐ and intra‐individual variations in seasonal and daily stabilities of the human gut microbiota in Japanese. Arch. Microbiol. 197:919–934.
    1. Human Microbiome Project C . 2012. Structure function and diversity of the healthy human microbiome. Nature 486:207–214.
    1. Jackson, M. A. , Jeffery I. B., Beaumont M., Bell J. T., Clark A. G., Ley R. E., et al. 2016. Signatures of early frailty in the gut microbiota. Genome Med. 8:8.
    1. Jones, B. , and Kenward M. G.. 2014. Design and Analysis of Cross‐Over Trials, 3rd ed. CRC Press, Boca Raton, FL.
    1. Kaakoush, N. O. , Martire S. I., Raipuria M., Mitchell H. M., Nielsen S., Westbrook R. F., et al. 2017. Alternating or continuous exposure to cafeteria diet leads to similar shifts in gut microbiota compared to chow diet. Mol. Nutr. Food Res. 61:1–2.
    1. Kawano, H. , Iemitsu M., Gando Y., Ishijima T., Asaka M., Aoyama T., et al. 2012. Habitual rowing exercise is associated with high physical fitness without affecting arterial stiffness in older men. J. Sports Sci. 30:241–246.
    1. Kelly, C. P. , and LaMont J. T.. 2008. Clostridium difficile–more difficult than ever. N. Engl. J. Med. 359:1932–1940.
    1. Kelly, T. N. , Bazzano L. A., Ajami N. J., He H., Zhao J., Petrosino J. F., et al. 2016. Gut microbiome associates with lifetime cardiovascular disease risk profile among bogalusa heart study participants. Circ. Res. 119:956–964.
    1. Kobayashi, S. , Honda S., Murakami K., Sasaki S., Okubo H., Hirota N., et al. 2012. Both comprehensive and brief self‐administered diet history questionnaires satisfactorily rank nutrient intakes in Japanese adults. J. Epidemiol. 22:151–159.
    1. Kodama, S. , Saito K., Tanaka S., Maki M., Yachi Y., Asumi M., et al. 2009. Cardiorespiratory fitness as a quantitative predictor of all‐cause mortality and cardiovascular events in healthy men and women: a meta‐analysis. JAMA 301:2024–2035.
    1. Konikoff, T. , and Gophna U.. 2016. Oscillospira: a central, enigmatic component of the human gut microbiota. Trends Microbiol. 24:523–524.
    1. Langille, M. G. , Zaneveld J., Caporaso J. G., McDonald D., Knights D., Reyes J. A., et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31:814–821.
    1. Larsen, N. , Vogensen F. K., van den Berg F. W., Nielsen D. S., Andreasen A. S., Pedersen B. K., et al. 2010. Gut microbiota in human adults with type 2 diabetes differs from non‐diabetic adults. PLoS ONE 5:e9085.
    1. Le Chatelier, E. , Nielsen T., Qin J., Prifti E., Hildebrand F., Falony G., et al. 2013. Richness of human gut microbiome correlates with metabolic markers. Nature 500:541–546.
    1. Lessa, F. C. , Mu Y., Bamberg W. M., Beldavs Z. G., Dumyati G. K., Dunn J. R., et al. 2015. Burden of Clostridium difficile infection in the United States. N. Engl. J. Med. 372:825–834.
    1. Leung, J. , Burke B., Ford D., Garvin G., Korn C., Sulis C., et al. 2013. Possible association between obesity and Clostridium difficile infection. Emerg. Infect. Dis. 19:1791–1798.
    1. Lewington, S. , Clarke R., Qizilbash N., Peto R., and Collins R.. 2002. Age‐specific relevance of usual blood pressure to vascular mortality: a meta‐analysis of individual data for one million adults in 61 prospective studies. Lancet 360:1903–1913.
    1. Li, J. , Zhao F., Wang Y., Chen J., Tao J., Tian G., et al. 2017. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 5:14.
    1. Lozupone, C. , and Knight R.. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228–8235.
    1. Martinez‐Caro, D. , Alegria E., Lorente D., Azpilicueta J., Calabuig J., and Ancin R.. 1984. Diagnostic value of stress testing in the elderly. Eur. Heart J. 5(Suppl E):63–67.
    1. McArdle, B. H. , and Anderson M. J.. 2001. Fitting multivariate models to community data : a comment on distance‐based redundancy analysis. Ecology 82:290–297.
    1. Montassier, E. , Gastinne T., Vangay P., Al‐Ghalith G. A., Bruley des Varannes S., Massart S., et al. 2015. Chemotherapy‐driven dysbiosis in the intestinal microbiome. Aliment. Pharmacol. Ther. 42:515–528.
    1. Ogata, H. , Goto S., Sato K., Fujibuchi W., Bono H., and Kanehisa M.. 1999. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27:29–34.
    1. O'Toole, P. W. , and Jeffery I. B.. 2015. Gut microbiota and aging. Science 350:1214–1215.
    1. Pluznick, J. L. 2017. Microbial short‐chain fatty acids and blood pressure regulation. Curr. Hypertens. Rep. 19:25.
    1. Qin, J. , Li Y., Cai Z., Li S., Zhu J., Zhang F., et al. 2012. A metagenome‐wide association study of gut microbiota in type 2 diabetes. Nature 490:55–60.
    1. Rupnik, M. , Wilcox M. H., and Gerding D. N.. 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7:526–536.
    1. Santisteban, M. M. , Qi Y., Zubcevic J., Kim S., Yang T., Shenoy V., et al. 2017. Hypertension‐linked pathophysiological alterations in the gut. Circ. Res. 120:312–323.
    1. Shannon, C. E. 1948. A mathematical theory of communication. Bell Labs Tech. J. 27:379–423.
    1. Shirai, K. , Utino J., Otsuka K., and Takata M.. 2006. A novel blood pressure‐independent arterial wall stiffness parameter; cardio‐ankle vascular index (CAVI). J. Atheroscler. Thromb. 13:101–107.
    1. Swain, D. P. , Abernathy K. S., Smith C. S., Lee S. J., and Bunn S. A.. 1994. Target heart rates for the development of cardiorespiratory fitness. Med. Sci. Sports Exerc. 26:112–116.
    1. Taniguchi, H. , Tanisawa K., Sun X., Kubo T., and Higuchi M.. 2016. Endurance exercise reduces hepatic fat content and serum fibroblast growth factor 21 levels in elderly men. J. Clin. Endocrinol. Metab. 101:191–198.
    1. Team, R. D. C. 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
    1. Tims, S. , Derom C., Jonkers D. M., Vlietinck R., Saris W. H., Kleerebezem M., et al. 2013. Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 7:707–717.
    1. Turnbaugh, P. J. , Hamady M., Yatsunenko T., Cantarel B. L., Duncan A., Ley R. E., et al. 2009. A core gut microbiome in obese and lean twins. Nature 457:480–484.
    1. Turnbaugh, P. J. , Quince C., Faith J. J., McHardy A. C., Yatsunenko T., Niazi F., et al. 2010. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc. Natl Acad. Sci. USA 107:7503–7508.
    1. Voreades, N. , Kozil A., and Weir T. L.. 2014. Diet and the development of the human intestinal microbiome. Front. Microbiol. 5:494.
    1. Walters, W. A. , Xu Z., and Knight R.. 2014. Meta‐analyses of human gut microbes associated with obesity and IBD. FEBS Lett. 588:4223–4233.
    1. Yang, T. , Santisteban M. M., Rodriguez V., Li E., Ahmari N., Carvajal J. M., et al. 2015. Gut dysbiosis is linked to hypertension. Hypertension 65:1331–1340.
    1. Yatsunenko, T. , Rey F. E., Manary M. J., Trehan I., Dominguez‐Bello M. G., Contreras M., et al. 2012. Human gut microbiome viewed across age and geography. Nature 486:222–227.
    1. Zhu, L. , Baker S. S., Gill C., Liu W., Alkhouri R., Baker R. D., et al. 2013. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57:601–609.

Source: PubMed

3
구독하다