The effect of resistance training on gut microbiota composition has not been explored, despite the evidence about endurance exercise. The aim of this study was to compare the effect of resistance and endurance training on gut microbiota composition in mice.
Methods: Cecal samples were collected from 26 C57BL/6N mice, divided into three groups: sedentary (CTL), endurance training on a treadmill (END), and resistance training on a vertical ladder (RES). After 2 weeks of adaption, mice were trained for 4 weeks, 5 days/week. Maximal endurance and resistance capacity test were performed before and after training. Genomic DNA was extracted and 16S Ribosomal RNA sequenced for metagenomics analysis. The percentages for each phylum, class, order, family, or genus/species were obtained using an open-source bioinformatics pipeline.
Results: END showed higher diversity and evenness. Significant differences among groups in microbiota composition were only observed at genera and species level. END showed a significantly higher relative abundance of Desulfovibrio and Desulfovibrio sp., while Clostridium and C. cocleatum where higher for RES.
Trained mice showed significantly lower relative abundance of Ruminococcus gnavus and higher of the genus Parabacteroides compared to CTL. We explored the relationship between relative taxa abundance and maximal endurance and resistance capacities after the training period.
Lachnospiraceae and Lactobacillaceae families were negatively associated with endurance performance, while several taxa, including Prevotellaceae family, Prevotella genus, and Akkermansia muciniphila, were positively correlated. About resistance performance, Desulfovibrio sp. was negatively correlated, while Alistipes showed a positive correlation.
Conclusion: Resistance and endurance training differentially modify gut microbiota composition in mice, under a high-controlled environment. Interestingly, taxa associated with anti- and proinflammatory responses presented the same pattern after both models of exercise. Furthermore, the abundance of several taxa was differently related to maximal endurance or resistance performance, most of them did not respond to training.
Authors: Javier Fernández1,2,3†, Manuel Fernández-Sanjurjo2,4†, Eduardo Iglesias-Gutiérrez2,4, Pablo Martínez-Camblor5, Claudio J. Villar1,2,3, Cristina Tomás-Zapico2,4*, Benjamin Fernández-García2,6‡ and Felipe Lombó1,2,3‡
- 1Department of Functional Biology, Microbiology, University of Oviedo, Oviedo, Spain
- 2Health Research Institute of the Principality of Asturias (ISPA), Oviedo, Spain
- 3Instituto Universitario de Oncología del Principado de Asturias (IUOPA), University of Oviedo, Oviedo, Spain
- 4Department of Functional Biology, Physiology, University of Oviedo, Oviedo, Spain
- 5Department of Biomedical Data Science, Geisel School of Medicine at Dartmouth, Hanover, NH, United States
- 6Department of Morphology and Cell Biology, Anatomy, University of Oviedo, Oviedo, Spain
Data Availability Statement
The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found at: https://www.ncbi.nlm.nih.gov/, PRJNA558220.
The animal study was reviewed and approved by the Research Ethics Committee of the University of Oviedo, Spain (PROAE 10/2016).
JF and MF-S performed the experiments, analyzed the data, and wrote the manuscript. CT-Z and PM-C analyzed the data, prepared the figures, and wrote the manuscript. CJV analyzed the data. EI-G, FL, and BF-G designed and supervised the study and wrote the manuscript. All authors have read and approved the final version of the manuscript and agree with the order of the presentation of the authors.
This work was supported by Ministerio de Economía y Competitividad under Grant DEP2015-69980-P to BF-G and by Programa de Ayudas a Grupos de Investigación del Principado de Asturias to FL (FC-GRUPIN-IDI/2018/000120).
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
The authors acknowledge the technical support provided by Servicios Científico-Técnicos de la Universidad de Oviedo and the Biostatistics and Epidemiology Unit from ISPA.
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fphys.2021.748854/full#supplementary-material
Allen, J. M., Berg Miller, M. E., Pence, B. D., Whitlock, K., Nehra, V., Gaskins, H. R., et al. (2015). Voluntary and forced exercise differentially alters the gut microbiome in C57BL/6J mice. J. Appl. Physiol. 118, 1059–1066. doi: 10.1152/japplphysiol.01077.2014
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. doi: 10.1249/MSS.0000000000001495
Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., et al. (2011). Enterotypes of the human gut microbiome. Nature 473, 174–180. doi: 10.1038/nature09944
Barcena, C., Valdes-Mas, R., Mayoral, P., Garabaya, C., Durand, S., Rodriguez, F., et al. (2019). Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice. Nat. Med. 25, 1234–1242. doi: 10.1038/s41591-019-0504-5
Barton, W., Penney, N. C., Cronin, O., Garcia-Perez, I., Molloy, M. G., Holmes, E., et al. (2018). The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level. Gut 67, 625–633. doi: 10.1136/gutjnl-2016-313627
Boureau, H., Decre, D., Carlier, J. P., Guichet, C., and Bourlioux, P. (1993). Identification of a Clostridium cocleatum strain involved in an anti-Clostridium difficile barrier effect and determination of its mucin-degrading enzymes. Res. Microbiol. 144, 405–410. doi: 10.1016/0923-2508(93)90198-B
Bycura, D., Santos, A. C., Shiffer, A., Kyman, S., Winfree, K., Sutliffe, J., et al. (2021). Impact of different exercise modalities on the human gut microbiome. Sports 9:14. doi: 10.3390/sports9020014
Campbell, S. C., Wisniewski, P. J., Noji, M., Mcguinness, L. R., Haggblom, M. M., Lightfoot, S. A., et al. (2016). The effect of diet and exercise on intestinal integrity and microbial diversity in mice. PLoS One 11:e0150502. doi: 10.1371/journal.pone.0150502
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. doi: 10.1038/nmeth.f.303
Carbajo-Pescador, S., Porras, D., Garcia-Mediavilla, M. V., Martinez-Florez, S., Juarez-Fernandez, M., Cuevas, M. J., et al. (2019). Beneficial effects of exercise on gut microbiota functionality and barrier integrity, and gut-liver crosstalk in an in vivo model of early obesity and non-alcoholic fatty liver disease. Dis. Model. Mech. 12:dmm039206. doi: 10.1242/dmm.039206
Chen, H., Shen, L., Liu, Y., Ma, X., Long, L., Ma, X., et al. (2021). Strength exercise confers protection in central nervous system autoimmunity by altering the gut microbiota. Front. Immunol. 12:628629. doi: 10.3389/fimmu.2021.628629
Choi, J. J., Eum, S. Y., Rampersaud, E., Daunert, S., Abreu, M. T., and Toborek, M. (2013). Exercise attenuates PCB-induced changes in the mouse gut microbiome. Environ. Health Perspect. 121, 725–730. doi: 10.1289/ehp.1306534
Codina-Martinez, H., Fernandez-Garcia, B., Diez-Planelles, C., Fernandez, A. F., Higarza, S. G., Fernandez-Sanjurjo, M., et al. (2020). Autophagy is required for performance adaptive response to resistance training and exercise-induced adult neurogenesis. Scand. J. Med. Sci. Sports 30, 238–253. doi: 10.1111/sms.13586
Colston, T. J., and Jackson, C. R. (2016). Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol. Ecol. 25, 3776–3800. doi: 10.1111/mec.13730
Conner, J. D., Wolden-Hanson, T., and Quinn, L. S. (2014). Assessment of murine exercise endurance without the use of a shock grid: an alternative to forced exercise. J. Vis. Exp. 90:e51846. doi: 10.3791/51846
Crovesy, L., Masterson, D., and Rosado, E. L. (2020). Profile of the gut microbiota of adults with obesity: a systematic review. Eur. J. Clin. Nutr. 74, 1251–1262. doi: 10.1038/s41430-020-0607-6
Das, A., Huang, G. X., Bonkowski, M. S., Longchamp, A., Li, C., Schultz, M. B., et al. (2018). Impairment of an endothelial NAD(+)-H2S signaling network is a reversible cause of vascular aging. Cell 173, 74.e20–89.e20. doi: 10.1016/j.cell.2018.02.008
Davidson, R. M., and Epperson, L. E. (2018). Microbiome sequencing methods for studying human diseases. Methods Mol. Biol. 1706, 77–90. doi: 10.1007/978-1-4939-7471-9_5
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. doi: 10.1371/journal.pone.0092193
Fernandez, J., Garcia, L., Monte, J., Villar, C. J., and Lombo, F. (2018). Functional anthocyanin-rich sausages diminish colorectal cancer in an animal model and reduce pro-inflammatory bacteria in the intestinal microbiota. Genes (Basel) 9:133. doi: 10.3390/genes9030133
Fernandez-Sanjurjo, M., Fernandez, J., Tomas-Zapico, C., Fernandez-Garcia, B., Villar, C. J., Lombo, F., et al. (2020). Is physical performance (in mice) increased by Veillonella atypica or decreased by Lactobacillus bulgaricus? J. Sport Health Sci. 9, 197–200. doi: 10.1016/j.jshs.2020.02.005
Figueiredo, V. C., De Salles, B. F., and Trajano, G. S. (2018). Volume for muscle hypertrophy and health outcomes: the most effective variable in resistance training. Sports Med. 48, 499–505. doi: 10.1007/s40279-017-0793-0
Fiuza-Luces, C., Garatachea, N., Berger, N. A., and Lucia, A. (2013). Exercise is the real polypill. Physiology 28, 330–358. doi: 10.1152/physiol.00019.2013
Flint, H. J., Duncan, S. H., Scott, K. P., and Louis, P. (2015). Links between diet, gut microbiota composition and gut metabolism. Proc. Nutr. Soc. 74, 13–22. doi: 10.1017/S0029665114001463
Gentil, P., Marques, V. A., Neto, J. P. P., Santos, A. C. G., Steele, J., Fisher, J., et al. (2018). Using velocity loss for monitoring resistance training effort in a real-world setting. Appl. Physiol. Nutr. Metab. 43, 833–837. doi: 10.1139/apnm-2018-0011
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. doi: 10.1016/j.cell.2014.09.053
Grogan, M. D., Bartow-Mckenney, C., Flowers, L., Knight, S. A. B., Uberoi, A., and Grice, E. A. (2019). Research techniques made simple: profiling the skin microbiota. J. Invest. Dermatol. 139, 747.e1–752.e1. doi: 10.1016/j.jid.2019.01.024
Hawley, J. A., Hargreaves, M., Joyner, M. J., and Zierath, J. R. (2014). Integrative biology of exercise. Cell 159, 738–749. doi: 10.1016/j.cell.2014.10.029
Hildebrand, F., Nguyen, T. L., Brinkman, B., Yunta, R. G., Cauwe, B., Vandenabeele, P., et al. (2013). Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 14:R4. doi: 10.1186/gb-2013-14-1-r4
Hsu, Y. J., Chiu, C. C., Li, Y. P., Huang, W. C., Huang, Y. T., Huang, C. C., et al. (2015). Effect of intestinal microbiota on exercise performance in mice. J. Strength Cond. Res. 29, 552–558. doi: 10.1519/JSC.0000000000000644
Johnson, K. V., and Burnet, P. W. (2016). Microbiome: should we diversify from diversity? Gut Microbes 7, 455–458. doi: 10.1080/19490976.2016.1241933
Kemi, O. J., Loennechen, J. P., Wisloff, U., and Ellingsen, O. (2002). Intensity-controlled treadmill running in mice: cardiac and skeletal muscle hypertrophy. J. Appl. Physiol. 93, 1301–1309. doi: 10.1152/japplphysiol.00231.2002
Knab, A. M., Bowen, R. S., Moore-Harrison, T., Hamilton, A. T., Turner, M. J., and Lightfoot, J. T. (2009). Repeatability of exercise behaviors in mice. Physiol. Behav. 98, 433–440. doi: 10.1016/j.physbeh.2009.07.006
Kregel, K. C., Allen, D. L., Booth, F. W., Fleshner, M. R., Henriksen, E. J., Musch, T. I., et al. (2006). Resource book for the design of animal exercise protocols. Am. J. Vet. Res. 68:583. doi: 10.2460/ajvr.68.6.583
Lamoureux, E. V., Grandy, S. A., and Langille, M. G. I. (2017). Moderate exercise has limited but distinguishable effects on the mouse microbiome. mSystems 2, e00006–e00017. doi: 10.1128/mSystems.00006-17
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. doi: 10.1038/nature12506
Lee, H., and Ko, G. (2014). Effect of metformin on metabolic improvement and gut microbiota. Appl. Environ. Microbiol. 80, 5935–5943. doi: 10.1128/AEM.01357-14
Ley, R. E., Backhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., and Gordon, J. I. (2005). Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U. S. A. 102, 11070–11075. doi: 10.1073/pnas.0504978102
Marteau, P., Pochart, P., Dore, J., Bera-Maillet, C., Bernalier, A., and Corthier, G. (2001). Comparative study of bacterial groups within the human cecal and fecal microbiota. Appl. Environ. Microbiol. 67, 4939–4942. doi: 10.1128/AEM.67.10.4939-4942.2001
McKenna, C. F., Salvador, A. F., Hughes, R. L., Scaroni, S. E., Alamilla, R. A., Askow, A. T., et al. (2021). Higher protein intake during resistance training does not potentiate strength, but modulates gut microbiota, in middle-aged adults: a randomized control trial. Am. J. Physiol. Endocrinol. Metab. 320, E900–E913. doi: 10.1152/ajpendo.00574.2020
Mohr, A. E., Jager, R., Carpenter, K. C., Kerksick, C. M., Purpura, M., Townsend, J. R., et al. (2020). The athletic gut microbiota. J. Int. Soc. Sports Nutr. 17:24. doi: 10.1186/s12970-020-00353-w
Myers, J., Prakash, M., Froelicher, V., Do, D., Partington, S., and Atwood, J. E. (2002). Exercise capacity and mortality among men referred for exercise testing. N. Engl. J. Med. 346, 793–801. doi: 10.1056/NEJMoa011858
Nguyen, T. L., Vieira-Silva, S., Liston, A., and Raes, J. (2015). How informative is the mouse for human gut microbiota research? Dis. Model. Mech. 8, 1–16. doi: 10.1242/dmm.017400
O’toole, P. W., and Jeffery, I. B. (2015). Gut microbiota and aging. Science 350, 1214–1215. doi: 10.1126/science.aac8469
Parker, B. J., Wearsch, P. A., Veloo, A. C. M., and Rodriguez-Palacios, A. (2020). The genus Alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front. Immunol. 11:906. doi: 10.3389/fimmu.2020.00906
Pedersen, B. K., and Saltin, B. (2015). Exercise as medicine – evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand. J. Med. Sci. Sports 25(Suppl. 3), 1–72. doi: 10.1111/sms.12581
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. doi: 10.1038/nature11450
Rothschild, D., Weissbrod, O., Barkan, E., Kurilshikov, A., Korem, T., Zeevi, D., et al. (2018). Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215. doi: 10.1038/nature25973
Scheiman, J., Luber, J. M., Chavkin, T. A., Macdonald, T., Tung, A., Pham, L. D., et al. (2019). Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat. Med. 25, 1104–1109. doi: 10.1038/s41591-019-0485-4
Tang, W. H. W., Li, D. Y., and Hazen, S. L. (2019). Dietary metabolism, the gut microbiome, and heart failure. Nat. Rev. Cardiol. 16, 137–154. doi: 10.1038/s41569-018-0108-7
Westcott, W. L. (2012). Resistance training is medicine: effects of strength training on health. Curr. Sports Med. Rep. 11, 209–216. doi: 10.1249/JSR.0b013e31825dabb8
Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y. Y., Keilbaugh, S. A., et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108. doi: 10.1126/science.1208344
Zhao, X., Zhang, Z., Hu, B., Huang, W., Yuan, C., and Zou, L. (2018). Response of gut microbiota to metabolite changes induced by endurance exercise. Front. Microbiol. 9:765. doi: 10.3389/fmicb.2018.00765
Keywords: resistance exercise, endurance exercise, murine models, metagenomics, physical performance
Citation: Fernández J, Fernández-Sanjurjo M, Iglesias-Gutiérrez E, Martínez-Camblor P, Villar CJ, Tomás-Zapico C, Fernández-García B and Lombó F (2021) Resistance and Endurance Exercise Training Induce Differential Changes in Gut Microbiota Composition in Murine Models. Front. Physiol. 12:748854. doi: 10.3389/fphys.2021.748854
Received: 09 August 2021; Accepted: 01 December 2021;
Published: 24 December 2021.
Silvia Turroni, University of Bologna, Italy
Copyright © 2021 Fernández, Fernández-Sanjurjo, Iglesias-Gutiérrez, Martínez-Camblor, Villar, Tomás-Zapico, Fernández-García and Lombó. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Cristina Tomás-Zapico, firstname.lastname@example.org
†These authors have contributed equally to this work and share first authorship
‡These authors have contributed equally to this work and share senior authorship
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