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Editorial

Exercise and Sport Sciences Reviews: 2019 Paper of the Year

Campbell, Sara C.

Author Information
Exercise and Sport Sciences Reviews: October 2020 - Volume 48 - Issue 4 - p 149-150
doi: 10.1249/JES.0000000000000228
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Editor’s note: The inaugural Paper of the Year for Exercise and Sport Sciences Reviews was selected based on the significance and impact of the article. To read more about the award and the articles selected for the other four journals published by the American College of Sports Medicine, seehttps://www.multibriefs.com/briefs/acsm/Active060220.htm.

EXERCISE AND THE MICROBIOME: EMERGING SCIENCE AND FUTURE OUTLOOK

It is with warm congratulations and excitement that this commentary is written in recognition of “Exercise and the gut microbiome: a review of the evidence, potential mechanisms, and implications for human health” being named Exercise and Sport Sciences Reviews paper of the year for 2019 (1). This work highlights the emerging science investigating the role of exercise training in manipulating the gut microbiome.

Although the study of microbiology has been around for centuries, only in the last few decades have scientists begun to aggressively pursue the role of gut microbes in human health. It is now widely accepted that these microorganisms play a powerful role in human health outcomes, ranging from obesity and diabetes to anxiety and depression. Although most of the research focuses on diet, the growing niche of the exercise microbiome deserves recognition. It has been shown by our group and others that exercise alters the microbiome independent of diet (2,3). Recently, our group has further shown that exercise exerts strain level selection for microbes within the host more robustly than genotype (4). In addition, studies have shown that depletion of the microbiome via antibiotics or the use of germ-free mice demonstrates a reduced exercise tolerance, suggesting that an intact microbiome is essential for exercise capacity (5). Together, these studies illustrate not only the immense independent impact exercise has on microbial community structure but also that exercise tolerance is indeed dependent on these microbes, highlighting a true symbiosis between host and its microbiome.

One of the exciting highlights of Mailing et al. (1), as noted in Figure 3, are the many proposed mechanisms by which exercise can alter the gut microbiome. One of the most documented alterations is the favorable increase in butyrate concentrations (6), butyrate-producing microbes (2), and the activity of butyryl CoA:acetate-CoA transferase (7). Butyrate is known for being beneficial for colonocyte proliferation and differentiation, which can help with inflammatory bowel disease–related outcomes. Mailing et al. also address the importance of the gut-immune interaction via gut-associated lymphoid tissue, or GALT, the impact of exercise of gut permeability, bile acid circulation, and metabolic flux. As the review highlights, all of these mechanisms have the potential to influence host metabolism, and understanding how these systems act both independently and interdependently will lead to meaningful discoveries for human health. Future studies should focus on the use of various -omic-based technologies to more accurately measure and quantify microbial derived metabolic by-products in systemic circulation. Only then can we truly link the microbiome causally to systemic health outcomes. Finally, use of technologies to enhance taxonomic resolution to ascertain which specific species/strains of microbes change with exercise will provide targets for therapeutic interventions. A known and excellent example of this is Fecalibacterium prausnitzii. F. prausnitzii has not only shown to be enhanced with exercise training (2,7) and with insulin administration improving type 2 diabetes outcomes (8), but also is associated with lower depression/anxiety scores on self-reported surveys (9). Given that exercise has positive health benefits on type 2 diabetes and mental health outcomes, making connections via the microbiome is an exciting way to overlap complementary areas of study.

An additional exciting area is the notion that the microbiome be considered a training adaptation. Accumulating evidence suggests that if you maintain exercise training, you can maintain the beneficial changes to the microbiome. Allen et al. (7), also from the Wood’s laboratory with Mailing et al., showed that exercise increased butyrate levels as well as fecal acetate and butyrate levels in lean and obese individuals. Interestingly, although these changes were dependent on body mass index status, short-chain fatty acid levels returned to normal when individuals returned to a sedentary state. Likewise, a recent article by Hampton-Marcell et al. (10) reported that in swimmers, coinciding with the decrease in training volume, the microbial community structure showed a significant decrease in overall microbial diversity, a decrease in microbial community structure similarity, and a decrease in the proportion of the bacterial genera Faecalibacterium and Coprococcus. These studies among a few others show that exercise training is required to maintain beneficial changes in the microbiome or they will revert back to the original “seeded” communities. More research is needed to understand the mechanisms that link both the timeline of these changes after exercise interventions and the reversal of these effects after detraining.

Mailing et al. concludes, “Ultimately, we can imagine a future of personalized microbiome-based lifestyle medicine, where baseline gut microbiota, diet, and other host factors might help predict which exercise program might be most effective for a given individual.” We share in the excitement of this statement and will continue to pursue this avenue of research with rigor. For now, congratulations on a job well done and continued success in moving this field forward!

Sara C. Campbell
Department of Kinesiology and Health
Rutgers University
New Brunswick, NJ

References

1. Mailing LJ, Allen JM, Buford TW, et al. Exercise and the gut microbiome: a review of the evidence, potential mechanisms, and implications for human health. Exerc. Sport Sci. Rev. 2019; 47:75–85.
2. 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.
3. Allen JM, Miller MEB, Pence BD, et al. Voluntary and forced exercise differentially alters the gut microbiome in C57BL/6J mice. J. Appl. Physiol. 2015; 118:1059–66.
4. Dowden RA, McGuinness LR, Wisniewski PJ, et al. Host genotype and exercise exhibit species-level selection for members of the gut bacterial communities in the mouse digestive system. Sci. Rep. 2020; 10:8984.
5. Hsu YJ, Chiu CC, Li YP, et al. Effect of intestinal microbiota on exercise performance in mice. J. Strength Cond. Res. 2015; 29:552–8.
6. 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; 72:572–6.
7. Allen JM, Mailing LJ, Niemiro GM, et al. Exercise alters gut microbiota composition and function in lean and obese humans. Med. Sci. Sports Exerc. 2018; 50:747–57.
8. Zhao L, Zhang F, Ding X, et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science. 2018; 359:1151–6.
9. Valles-Colomer M, Falony G, Darzi Y, et al. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat. Microbiol. 2019; 4:623–32.
10. Hampton-Marcell TJ, Eshoo TW, Cook MD, et al. Comparative analysis of gut microbiota following changes in training volume among swimmers. Int. J. Sports Med. 2020; 41:292–9.
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