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Alex Mohr

Can the gut microbiota be trained?

Athletes that follow an exercise and dietary regimen usually expect to see a performance benefit for their efforts. Also impacted by these factors are the microbes harbored in the gut, called the gut microbiota. In Part I of this series, we covered how this community of microbes responds to exercise and diet. This is part 2: Here we explore how such stimuli might modify this community in a way to support athletic performance. A sort of “training” if you will.

The gut-muscle axis

The impact of exercise

There is evidence that exercise promotes changes in the structure of the gut, though this appears to vary greatly depending on the exercise intensity, mode, and time (1). While longitudinal data is generally limited in humans, some very intriguing work has been conducted using rodents. For example, mice undergoing moderate-intensity treadmill exercise for several months had a significant alteration in their core microbiota and associated metabolic activity, paralleling increased exercise performance (2). There was a notable increase in the bacterial genera Bifidobacteria, often used in probiotics, in the exercised mice. Interestingly this was correlated with enhanced metabolic activities related to exercise, including glucose metabolism.


To better determine a causal link and explore the importance of the gut microbiota, several research groups have used antibiotics to effectively kill off a significant portion of gut bacteria and then subjected animals to exercise. In comparison to baseline exercise performance, where mice had an intact gut microbiota, heavy antibiotic treatment resulted in large decreases in running capacity and muscle function (3, 4). Such work showcases an emerging concept, termed the ‘gut-muscle axis’, that highlights the bi-directional relationship between muscle tissue and the gut microbiota (5). Demonstrating that this relationship is in fact a two-way street, one of the researcher groups took it one step further and also restored the gut bacteria of the antibiotically treated mice. Restoration of the gut flora reversed the decrements in endurance capacity and muscle function (3). Clearly, the gut microbiota can impact performance, but what about humans?


There is evidence from rodent studies of a bi-directional relationship between muscle tissue and the gut microbiota, termed the 'gut-muscle axis'.

In one of the more interesting and recent investigations, Barton and colleagues used a case-study approach, tracking the gut microbiotas of two sedentary male humans as they embarked on a 6-month training program for either a marathon or an Olympic-distance triathlon (6). As the training progressed, so did the participant’s body composition and fitness parameters. Increases in gut microbiota diversity (a health-associated feature) occurred with sustained training. The participants exhibited increased abundance of microbial species that have been shown to influence short-chain fatty acid (SCFA) production. SCFAs act as fuel substrates that have been shown previously to be taken up by the body and used in muscle tissue (7). Yet the increase in these SCFA-producing microbes was not reflected in actual SCFA levels. The authors stated it may take time for the metabolic alterations to emerge or the microbes were not getting enough nutrients via the participants’ diets.


Exercise or diet? Not so easy to distinguish

Exercise has the potential to modify the gut microbiota, but it is rather difficult to separate out other confounding factors like dietary intake. In relation to comparing differences in gut microbiotas, this has been highlighted in professional rugby athletes vs. sedentary controls (8). While these two groups were approximately the same body mass, the athletes consumed about 1,500 more calories and 140 grams more protein! Whether it be greater energy intake, high-carb, low-carb, increased protein, feeding strategies during exercise, etc., all can influence the composition and, ultimately, the function of the gut microbiome.


As noted in Part I, gut bacteria can break down complex carbohydrates, like dietary fiber, through fermentation processes ultimately producing SCFAs. This includes, acetate, propionate, and important for our discussion, butyrate. This SCFA is one of the primary sources of fuel for the cells that line our gastrointestinal tract. Forming the gut barrier, these cells have a short life cycle of a few days and need a substantial amount of energy and nutrients (9). By providing them with energy and nutrients, it follows that they may do their job better, and maintain better gastrointestinal health.


A problem many endurance-based athletes suffer from is gastrointestinal issues (10). Exercise stress, heat, and hydration methods aside, endurance athletes may benefit from optimizing the intake of gut-friendly carbohydrates.


A term that gets used in this space is microbiota-accessible carbohydrates, or MACs for short.

What are MACs?

MACs are carbohydrate that are not metabolised by the host and thus are available for metabolism by the microbiota. Diets low in MACs appear to promote the growth of bacteria that degrade the mucus lining around the gut barrier (11). This can impair the barrier integrity and cause issues. However, not everyone may respond well to a diet high in MACs right away. Common side effects may include bloating and gas (12). If your diet is low in MACs, it’s best to slowly increase these foods over time. And, very importantly, not close to exercise bouts.

"...endurance athletes may benefit from from optimizing the intake of [microbiota accessible carbohydrates, or MAC]… However, not everyone may respond well to a diet high in MACs right away."


A diet low in microbiota accessible carbohydrates may not get the benefits from SCFA production

Another group of athletes that deserves mentioning are those more aesthetically inclined, like bodybuilders. Depending on how close a bodybuilder is away from competition they may reduce total calorie intake, decrease relative carbohydrate and/or fat intake and increase relative protein intake. Assessing a group of male body builders following high-protein and low-dietary fiber diet, Jang and colleagues noted significant decreases in the abundance of beneficial microbes (13). Reflecting back to the professional rugby players, protein intake was actually positively correlated with microbial diversity, a feature recognized as “good” for gut health. Why might there be these two different findings? The rugby athletes actually met all of the recommended dietary intake requirements (8), while the bodybuilders did not (13). They consumed much less carbohydrate and fiber compared to standard intakes. While Jang and colleagues did not measure other analytes like SCFAs, it may be that these athletes could also benefit from increasing MACs, that are resistant to human enzymes but can be metabolized by select, health-associated bacteria in the gut. Moreover, the quality and digestibility of different protein sources may influence the site of digestion and absorption within the gut. Highly digestible proteins, such as whey, can be digested by host enzymes in upper intestines, reducing microbial fermentation farther down the digestive tract. Proteins of plant origin are available for microbial fermentation in a more distal site given incomplete digestion by host enzymes, particularly at a higher protein level. Evidence from animal research indicates proteins from vegetable origin have a more marked effect on microbial diversity than animal proteins (14), however investigation in athletes is needed.



Main takeaways

Exercise does appear to alter the structure of the gut microbiota, with some evidence suggesting it increases overall community diversity and the abundance of microbes that produce SCFAs. Substrates like these are linked to enhanced performance, improved recovery, reduced incidence of illness (15). Over time, as one becomes more fit, it may be that restructuring of the microbial community better serves host performance by supplying fuel and aiding exercise metabolism (7). However, to support these changes, diet also seems to be important. An emerging strategy may be for athletes to supplement their diet with MACs which may help encourage the growth of health-associated microbes. Another potential strategy may be the ingestion of fermented foods and probiotics, a topic we’ll discuss later.

How to look after your microbiome


The bottom line

While it is perhaps too early to provide concrete advice on how to modulate the microbiome to optimize performance/recovery, we do know diet and antibiotic use can have some of the most profound effects on the adult GM.

Therefore,

  1. athletes should take antibiotics under the guidance of their healthcare provider and not unnecessarily.

  2. athletes should consume a diversity of different foods and not eat the same thing everyday!

  3. opt for a variety of MACs away from intense training periods

  4. include some less digestible proteins (plant origin) in the diet

  5. maintain hydration to keep the GI tract functioning well


References:

  1. Mohr AE, Jäger R, Carpenter KC, Kerksick CM, Purpura M, Townsend JR, West NP, Black K, Gleeson M, Pyne DB, Wells SD, Arent SM, Kreider RB, Campbell BI, Bannock L, Scheiman J, Wissent CJ, Pane M, Kalman DS, Pugh JN, Ortega-Santos CP, Ter Haar JA, Arciero PJ, Antonio J. The athletic gut microbiota. J Int Soc Sports Nutr. 2020 May 12;17(1):24. doi: 10.1186/s12970-020-00353-w.

  2. Yang W, Liu Y, Yang G, Meng B, Yi Z, Yang G, Chen M, Hou P, Wang H, Xu X. Moderate-Intensity Physical Exercise Affects the Exercise Performance and Gut Microbiota of Mice. Front Cell Infect Microbiol. 2021 Sep 24;11:712381. doi: 10.3389/fcimb.2021.712381.

  3. Nay K, Jollet M, Goustard B, Baati N, Vernus B, Pontones M, Lefeuvre-Orfila L, Bendavid C, Rué O, Mariadassou M, Bonnieu A, Ollendorff V, Lepage P, Derbré F, Koechlin-Ramonatxo C. Gut bacteria are critical for optimal muscle function: a potential link with glucose homeostasis. Am J Physiol Endocrinol Metab. 2019 Jul 1;317(1):E158-E171. doi: 10.1152/ajpendo.00521.2018.

  4. Okamoto T, Morino K, Ugi S, Nakagawa F, Lemecha M, Ida S, Ohashi N, Sato D, Fujita Y, Maegawa H. Microbiome potentiates endurance exercise through intestinal acetate production. Am J Physiol Endocrinol Metab. 2019 May 1;316(5):E956-E966. doi: 10.1152/ajpendo.00510.2018.

  5. Przewłócka K, Folwarski M, Kaźmierczak-Siedlecka K, Skonieczna-Żydecka K, Kaczor JJ. Gut-Muscle AxisExists and May Affect Skeletal Muscle Adaptation to Training. Nutrients. 2020 May 18;12(5):1451. doi: 10.3390/nu12051451.

  6. Barton W, Cronin O, Garcia-Perez I, Whiston R, Holmes E, Woods T, Molloy CB, Molloy MG, Shanahan F, Cotter PD, O'Sullivan O. The effects of sustained fitness improvement on the gut microbiome: A longitudinal, repeated measures case-study approach. Transl Sports Med. 2021 Mar;4(2):174-192. doi: 10.1002/tsm2.215.

  7. Scheiman J, Luber JM, Chavkin TA, MacDonald T, Tung A, Pham LD, Wibowo MC, Wurth RC, Punthambaker S, Tierney BT, Yang Z, Hattab MW, Avila-Pacheco J, Clish CB, Lessard S, Church GM, Kostic AD. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med. 2019 Jul;25(7):1104-1109. doi: 10.1038/s41591-019-0485-4.

  8. Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, O'Reilly M, Jeffery IB, Wood-Martin R, Kerins DM, Quigley E, Ross RP, O'Toole PW, Molloy MG, Falvey E, Shanahan F, Cotter PD. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014 Dec;63(12):1913-20. doi: 10.1136/gutjnl-2013-306541.

  9. Arike L, Seiman A, van der Post S, Rodriguez Piñeiro AM, Ermund A, Schütte A, Bäckhed F, Johansson MEV, Hansson GC. Protein Turnover in Epithelial Cells and Mucus along the Gastrointestinal Tract Is Coordinated by the Spatial Location and Microbiota. Cell Rep. 2020 Jan 28;30(4):1077-1087.e3. doi: 10.1016/j.celrep.2019.12.068.

  10. PughJN, Kirk B, Fearn R, Morton JP, Close GL. Prevalence, Severity and Potential Nutritional Causes of Gastrointestinal Symptoms during a Marathon in Recreational Runners. Nutrients. 2018 Jun 24;10(7):811. doi: 10.3390/nu10070811.

  11. Daien CI, Pinget GV, Tan JK, Macia L. Detrimental impact of microbiota-accessible carbohydrate-deprived diet on gut and immune homeostasis: an overview. Front. Immunol. 2017; 8:548.

  12. de Oliveira EP, Burini RC, Jeukendrup A. Gastrointestinal complaints during exercise: prevalence, etiology, and nutritional recommendations. Sports Med. 2014; 44(Suppl. 1):S79–85.

  13. 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 May 3;16(1):21. doi: 10.1186/s12970-019-0290-y.

  14. 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 Apr;146(4):697-705. doi: 10.3945/jn.115.224196.

  15. Bongiovanni T, Yin MOL, Heaney L. The Athlete and Gut Microbiome: Short-chain Fatty Acids as Potential Ergogenic Aids for Exercise and Training. Int J Sports Med. 2021 Dec;42(13):1143-1158. doi: 10.1055/a-1524-2095.

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