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Does the gut microbiota play a role in exercise performance? Part 1

Most of the microorganisms that live on and inside us are contained in our digestive tract with increasing concentrations generally found the further down you go (💩). While research investigating these gut-specific microbes is still emerging, what is clear thus far, is this community is essential to our health. In relation, a recent and intriguing research area is aimed at assessing the potential linkage of these gut microbes with features of athleticism.


Gut microbiota and performance. A two way straat between physical activity and the gut microbiome.

What is the gut microbiota?

The gut microbiota is defined as diverse ecosystem consisting of (primarily) bacteria, archaea, viruses, protists, and even fungal communities all residing in the gastrointestinal tract (1). What we are trying to establish in this blog is how important factors like exercise and diet influence this community. And, for our own selfish desires, how does this community might benefit us. A sort of “two-way street” if you will.


Those that engage in regular exercise and have a specific diet regimen appear to have a community distinct from those more sedentary (2, 3). The structure of the athlete gut microbiota is likely, in part, the result of adaptations to these long‐term lifestyle factors (4). Indeed, athletes adhering to fairly spartan schedules for years and even decades are not uncommon.


What makes an athlete's gut microbiota "distinct"?

A key feature to highlight, in the context of athletes, is the role the gut has in producing short-chain fatty acids (SCFAs). These molecules can be used as a fuel substrate by the body and even act as signaling intermediates involved in the regulation of metabolism and inflammation (5). SCFAs are produced by the fermentation of non-digestible food components such as dietary fiber and other components, including those derived from our own bodies (6).


In comparison to sedentary individuals, athletes have increased fecal metabolites and improved overall health (unless over-trained or in energy deficiency) (7). While speculative, athletes may also possess gut microbiota “resilience”. What this refers to is the ability of the gut flora to return to “baseline” following stressful situations like extreme dietary or exercise pressures. This is recognized as an important feature of a health-associated gut community (8).


"In comparison to sedentary individuals, athletes have increased fecal metabolites and improved overall health (unless over-trained or in energy deficiency)".

What effect does exercise have on the gut microbiota?

In the last few years several research groups have been able to capture the effects of extreme exercise on the gut microbiota. For example, examining Boston marathon participant’s stool samples, Scheiman and colleagues noted an increase abundance of a microbe called Veillonella after the race (9). Through a series of experiments involving isolating a specific strain of Veillonella from participant’s stool, mice inoculated with this bacterium dramatically increased exercise performance. What appeared to be occurring was this microbe metabolized lactate (a metabolite of muscle metabolism) into SCFAs (a fuel source). Scheiman and colleagues theorized that higher levels of lactate in the gut of athletes might favor the growth of these bacteria which in turn could help aid performance. But exactly how this these bacteria are linked to improved performance is currently unknown.


SCFA-producing microbes have shown up in other investigations of endurance-based exercise events, including the grueling Western States Endurance Run, a 163 km mountain footrace. Here, changes in the gut microbiota of a world-class ultramarathon runner before and after competing were reported, showing a massive increase in Veillonella two hours post-race (10). In another extreme case, four well-trained male athletes had their gut microbiotas traced before, during, and after a continuous, unsupported 33-day, 5000 km transoceanic rowing race averaging close to 400 hours of rowing for each athlete (11). Increased abundance of SCFA (i.e., butyrate) producing species and species associated with improved metabolic health were noted.


Individual responses

More recently, two unfit males had their gut flora tracked for 6 months as they undertook progressive exercise training with one training for a marathon and the other an Olympic-distance triathlon (12). There were increases in health-associated metrics like community diversity and abundance of microbial species that have been shown to influence SCFA production. Importantly, these two participants had differential changes in specific health-associated microbes highlighting a very important feature of the human gut microbiota. It is individualized.


As with training adaptations, the response of the gut flora to exercise is likely quite variable and, as noted above, individual. Moreover, it is extremely hard to separate out factors like diet, especially since many athletes are on a very specific regimen (13). Finally, not all exercise stress is necessarily good for the gut. For example, athletes training at high intensities for long periods without adequate fueling are at risk for disturbances in gut integrity and function and gastrointestinal symptoms (14). These issues do raise some caution when looking at the athletic gut microbiota and generalizing findings.


"As with training adaptations, the response of the gut flora to exercise is likely quite variable and... individual".

So, does an athlete’s gut microbes help aid performance?

From the limited evidence, athletes as a group appear to harbor an increased abundance of functional pathways within the microbiota that could support exercise metabolism and athlete health (7). Like the SCFA-producing microbes and SCFA production noted. In some sense, the gut microbiota may be viewed as an energy harvester for athletes. Indeed, the digestive tract offers an incredibly large exchange surface area (80 m2!) for gut-derived metabolites (15).


In instances like endurance-based exercise, which can be extremely metabolically demanding, SCFA may be an important consideration for performance as they are readably absorbed into systemic circulation (16). These SCFAs can then be directly used in muscle and other tissues (17). In skeletal muscle, SCFAs can support energy metabolism during exercise (18). SCFAs also contribute to increased blood flow, insulin sensitivity, skeletal muscle mass preservation, and an oxidative phenotype (17).


The main takeaways...

The gut microbiota of athletes appears to have increased fecal metabolites like SCFAs, which may play a role in exercise performance and overall health compared to less active individuals (7). These differences are likely driven by the effects of exercise training and/or dietary intake. They may also have a greater ability to harness energy from the diet and products of exercise metabolism.


Overall, the mechanisms by which exercise may promote a rich bacterial community, increased functional pathways, and exercise-enhancing metabolites are not fully understood, but likely involve a multitude of factors beyond training and diet. Finally, most of the studies are correlative (we all know the adage; “correlation does not imply causation”). However, there is a growing interest in researching how the gut is modified by longitudinal designs and if the microbiota can be “trained”. A topic we cover in Part II.


References:

  1. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012 Jun 13;486(7402):207-14. doi: 10.1038/nature11234. PMID: 22699609; PMCID: PMC3564958.

  2. 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. Epub 2014 Jun 9. PMID: 25021423.

  3. Barton W, Penney NC, Cronin O, Garcia-Perez I, Molloy MG, Holmes E, Shanahan F, Cotter PD, O'Sullivan O. The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level. Gut. 2018 Apr;67(4):625-633. doi: 10.1136/gutjnl-2016-313627. Epub 2017 Mar 30. PMID: 28360096.

  4. O'Donovan CM, Madigan SM, Garcia-Perez I, Rankin A, O' Sullivan O, Cotter PD. Distinct microbiome composition and metabolome exists across subgroups of elite Irish athletes. J Sci Med Sport. 2020 Jan;23(1):63-68. doi: 10.1016/j.jsams.2019.08.290. Epub 2019 Sep 18. PMID: 31558359.

  5. Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol. 2014;121:91-119. doi: 10.1016/B978-0-12-800100-4.00003-9. PMID: 24388214.

  6. Blaak EE, Canfora EE, Theis S, Frost G, Groen AK, Mithieux G, Nauta A, Scott K, Stahl B, van Harsselaar J, van Tol R, Vaughan EE, Verbeke K. Short chain fatty acids in human gut and metabolic health. Benef Microbes. 2020 Sep 1;11(5):411-455. doi: 10.3920/BM2020.0057. Epub 2020 Aug 31. PMID: 32865024.

  7. 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. PMID: 32398103; PMCID: PMC7218537.

  8. Bäckhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM, Versalovic J, Young V, Finlay BB. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012 Nov 15;12(5):611-22. doi: 10.1016/j.chom.2012.10.012. PMID: 23159051.

  9. 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. Epub 2019 Jun 24. PMID: 31235964; PMCID: PMC7368972.

  10. Grosicki GJ, Durk RP, Bagley JR. Rapid gut microbiome changes in a world-class ultramarathon runner. Physiol Rep. 2019 Dec;7(24):e14313. doi: 10.14814/phy2.14313. PMID: 31872558; PMCID: PMC6928244.

  11. Keohane DM, Woods T, O'Connor P, Underwood S, Cronin O, Whiston R, O'Sullivan O, Cotter P, Shanahan F, Molloy MGM. Four men in a boat: Ultra-endurance exercise alters the gut microbiome. J Sci Med Sport. 2019 Sep;22(9):1059-1064. doi: 10.1016/j.jsams.2019.04.004. Epub 2019 Apr 18. PMID: 31053425.

  12. 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. Epub 2020 Dec 13. PMID: 34355132; PMCID: PMC8317196.

  13. Hughes RL. A Review of the Role of the Gut Microbiome in Personalized Sports Nutrition. Front Nutr. 2020 Jan 10;6:191. doi: 10.3389/fnut.2019.00191. PMID: 31998739; PMCID: PMC6966970.

  14. Pugh JN, 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. PMID: 29937533; PMCID: PMC6073243.

  15. Helander HF, Fändriks L. Surface area of the digestive tract - revisited. Scand J Gastroenterol. 2014 Jun;49(6):681-9. doi: 10.3109/00365521.2014.898326. Epub 2014 Apr 2. PMID: 24694282.

  16. Boets E, Gomand SV, Deroover L, Preston T, Vermeulen K, De Preter V, Hamer HM, Van den Mooter G, De Vuyst L, Courtin CM, Annaert P, Delcour JA, Verbeke KA. Systemic availability and metabolism of colonic-derived short-chain fatty acids in healthy subjects: a stable isotope study. J Physiol. 2017 Jan 15;595(2):541-555. doi: 10.1113/JP272613. Epub 2016 Sep 18. PMID: 27510655; PMCID: PMC5233652.

  17. Carey RA, Montag D. Exploring the relationship between gut microbiota and exercise: short-chain fatty acids and their role in metabolism. BMJ Open Sport Exerc Med. 2021 Apr 20;7(2):e000930. doi: 10.1136/bmjsem-2020-000930. PMID: 33981447; PMCID: PMC8061837.

  18. Bycura D, Santos AC, Shiffer A, Kyman S, Winfree K, Sutliffe J, Pearson T, Sonderegger D, Cope E, Caporaso JG. Impact of Different Exercise Modalities on the Human Gut Microbiome. Sports (Basel). 2021 Jan 21;9(2):14. doi: 10.3390/sports9020014. PMID: 33494210; PMCID: PMC7909775.

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