Comparative Analysis of Gut Microbiota Following Changes in Training Volume Among Swimmers

Abstract

Exercise can influence gut microbial community structure and diversity; however, the temporal dynamics of this association have rarely been explored. Here we characterized fecal microbiota in response to short term changes in training volume. Fecal samples, body composition, and training logs were collected from Division I NCAA collegiate swimmers during peak training through their in-season taper in 2016 (n=9) and 2017 (n=7), capturing a systematic reduction in training volume near the conclusion of their athletic season. Fecal microbiota were characterized using 16S rRNA V4 amplicon sequencing and multivariate statistical analysis, Spearman rank correlations, and random forest models. Peak training volume, measured as swimming distance, decreased significantly during the study period from 32.6±4.8 km/wk to 11.3±8.1 km/wk (ANOVA, p<0.05); however, body composition showed no significant changes. Coinciding with the decrease in training volume, the microbial community structure showed a significant decrease in overall microbial diversity, a decrease in microbial community structural similarity, and a decrease in the proportion of the bacterial genera Faecalibacterium and Coprococcus. Together these data demonstrate a significant association between short-term changes in training volume and microbial composition and structure in the gut; future research will establish whether these changes are associated with energy balance or nutrient intake.

Key words

gut microbiota - exercise - athletes - swimming

• References

• 1 Gilbert JA, Blaser MJ, Caporaso JG. et al. Current understanding of the human microbiome. Nat Med 2018; 24: 392-400
• 2 Faith JJ, Guruge JL, Charbonneau M. et al. The long-term stability of the human gut microbiota. Science 2013; 341: 1237439
• 3 Wu GD, Chen J, Hoffmann C. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334: 105-108
• 4 Flores GE, Caporaso JG, Henley JB. et al. Temporal variability is a personalized feature of the human microbiome. Genome Biol 2014; 15: 531
• 5 David LA, Materna AC, Friedman J. et al. Erratum to: Host lifestyle affects human microbiota on daily timescales. Genome Biol 2016; 17: 117
• 6 Rothschild D, Weissbrod O, Barkan E. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 2018; 555: 210-215
• 7 Matsumoto M, Inoue R, Tsukahara T. et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem 2008; 72: 572-576
• 8 Allen JM, Berg Miller ME, Pence BD. et al. Voluntary and forced exercise differentially alters the gut microbiome in C57BL/6J mice. J Appl Physiol (1985) 2015; 118: 1059-1066
• 9 Cook MD, Allen JM, Pence BD. 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: 158-163
• 10 Campbell SC, Wisniewski PJ, Noji M. et al. The Effect of Diet and Exercise on Intestinal Integrity and Microbial Diversity in Mice. PLoS One 2016; 11: e0150502
• 11 Scheiman J, Luber JM, Kostic AD. et al. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med 2019; 25: 1104-1109
• 12 Clarke SF, Murphy EF, O’Sullivan O. et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 2014; 63: 1913-1920
• 13 Estaki M, Pither J, Baumeister P. et al. Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. Microbiome 2016; 4: 42
• 14 Petersen LM, Bautista EJ, Nguyen H. et al. Community characteristics of the gut microbiomes of competitive cyclists. Microbiome 2017; 5: 98
• 15 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
• 16 Siri WE. Lawrence Radiation Laboratory, University of California, Berkeley. Body Composition from Fluid Spaces and Density: Analysis of Methods. Lawrence Radiation Laboratory, 1956.
• 17 McDonald D. et al. American Gut: an Open Platform for Citizen-Science Microbiome Research. bioRxiv. 2018; 277970 doi:10.1101/277970
• 18 Hamady M, Walker JJ, Harris JK. et al. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 2008; 5: 235-237
• 19 Caporaso JG, Lauber CL, Walters WA. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012; 6: 1621-1624
• 20 Caporaso JG, Kuczynski J, Stombaugh J. et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7: 335-336
• 21 McDonald D, Price MN, Goodrich J. et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 2012; 6: 610-618
• 22 Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26: 2460-2461
• 23 McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013; 8: e61217
• 24 Wickham H. ggplot2. WIREs Comp Stat 2011; 3: 180-185
• 25 Monda V, Villano I, Valenzano A et al. Exercise modifies the gut microbiota with positive health effects. Oxid Med Cell Longev 2017; 3831972
• 26 Ríos-Covián D, Ruas-Madiedo P, Margolles A. et al. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol 2016; 7: 185
• 27 Bressa C, Bailén-Andrino M, Pérez-Santiago J. et al. Differences in gut microbiota profile between women with active lifestyle and sedentary women. PLoS One 2017; 12: e0171352
• 28 Rosenbaum M, Knight R, Leibel RL. The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol Metab 2015; 26: 493-501
• 29 Kang SS, Jeraldo PR, Kurti A. et al. Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition. Mol Neurodegener 2014; 9: 36
• 30 Hoogenboom BJ, Morris J, Morris C. et al. Nutritional knowledge and eating behaviors of female, collegiate swimmers. N Am J Sports Phys Ther 2009; 4: 139-148
• 31 Shaw G, Boyd KT, Burke LM. et al. Nutrition for swimming. Int J Sports Nutr Exerc Metab 2014; 24: 360-372
• 32 Hinton PS, Sanford TC, Davidson MM. et al. Nutrient intakes and dietary behaviors of male and female collegiate athletes. Int J Sports Nutr Exerc Metab 2004; 14: 389-405
• 33 Evans CC, LePard KJ, Kwak JW. 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: e92193
• 34 Ley RE, Bäckhed F, Turnbaugh P. et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 2005; 102: 11070-11075