Fibrolytic efficiency of the large intestine microbiota may benefit running speed in French trotters: A pilot study.
Abstract: This pilot study sought to explore the contribution of the large intestine microbiota to energy metabolism and exercise performance through its ability to degrade fibers into short-chain fatty acids (SCFAs). To investigate this, a correlational study was carried out on athlete horses under the same management conditions. Fecal microbiota diversity and composition, fibrolytic efficiency and SCFAs were analyzed. An incremental running test was carried out to estimate the maximal running speed (MRS) of the horses, and blood samples were taken to measure energy metabolism parameters. MRS was positively correlated with the efficiency of the fecal microbiota in degrading cellulose in vitro (r = 0.51; p = 0.02). The abundance of fibrolytic bacterial taxa was not associated with MRS, but functional inference analysis revealed a positive association between MRS and pathways potentially related to fibrolytic activity (r = 0.54; p = 0.07 and r = 0.56; p = 0.05 for butyrate metabolism and thiamine metabolism, respectively). In contrast, the metabolic pathway of starch degradation appeared negatively associated with MRS (r = -0.55; p = 0.06). The present findings suggest a potential contribution of the large intestine microbiota and dietary fibers digestion to exercise capacity in equine athletes.
© 2024 The Author(s). Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.
Publication Date: 2024-11-13 PubMed ID: 39533164PubMed Central: PMC11557442DOI: 10.14814/phy2.70110Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research investigates the possible influence of large intestine bacteria in horses on energy metabolism and exercise performance by breaking down fibers into short-chain fatty acids (SCFAs). The study found a correlation between the run speed of athlete horses and the efficacy of their fecal microbes in breaking down cellulose.
Study participants and procedures
- The study was performed on athlete horses who were kept under the same management conditions. This helped eliminate variables related to diet, training, and living conditions that may affect the gut microbiota or the horses’ exercise performance.
- A series of tests were conducted to monitor the fecal microbiota, their ability to degrade fibers (fibrolytic efficiency), and the production of short-chain fatty acids (SCFAs).
- The researchers also performed an incremental running test to estimate the horses’ maximal running speed (MRS) and took blood samples to measure parameters associated with energy metabolism.
Results and findings
- There was a positive correlation observed between the maximal running speed of the horses and the efficiency of their fecal microbiota in breaking down cellulose. Essentially, the better the gut bacteria were at degrading fibers into SCFAs, the faster the horses could run.
- Interestingly, the abundance of fibrolytic bacteria – those that break down fibers – did not correlate with maximal running speed. Instead, some metabolic pathways related to fibrolytic activity showed a positive correlation with running speed.
- Notably, an association was found between maximal running speed and the metabolism pathways for butyrate and thiamine (vitamin B1). Butyrate is a type of SCFA that serves as a primary energy source for the cells lining the colon.
- Contrarily, the metabolic pathway of starch degradation appeared negatively associated with maximal running speed, suggesting that a more starch-oriented metabolism may not be favorable for running performance.
- In conclusion, the study suggests that gut microbiota’s efficiency in breaking down dietary fibers may influence exercise capacity in horses, possibly by affecting the horse’s energy metabolism.
Cite This Article
APA
Vasseur M, Lepers R, Langevin N, Julliand S, Grimm P.
(2024).
Fibrolytic efficiency of the large intestine microbiota may benefit running speed in French trotters: A pilot study.
Physiol Rep, 12(21), e70110.
https://doi.org/10.14814/phy2.70110 Publication
Researcher Affiliations
- Institut National de la Santé et de la Recherche Médicale, Inserm UMR 1093, Cognition Action et Plasticité Sensorimotrice (CAPS), Faculty of Sport Sciences, Université de Bourgogne, Dijon, France.
- Lab to Field, Dijon, France.
- Institut National de la Santé et de la Recherche Médicale, Inserm UMR 1093, Cognition Action et Plasticité Sensorimotrice (CAPS), Faculty of Sport Sciences, Université de Bourgogne, Dijon, France.
- Ecurie Hunter Valley, Belfonds, France.
- Lab to Field, Dijon, France.
- Lab to Field, Dijon, France.
MeSH Terms
- Animals
- Running / physiology
- Pilot Projects
- Gastrointestinal Microbiome / physiology
- Horses
- Feces / microbiology
- Male
- Physical Conditioning, Animal
- Fatty Acids, Volatile / metabolism
- Dietary Fiber / metabolism
- Dietary Fiber / administration & dosage
- Intestine, Large / microbiology
- Intestine, Large / metabolism
- Energy Metabolism / physiology
- Female
Grant Funding
- 2021/1600 / Association Nationale de la Recherche et de la Technologie (ANRT)
- 1 / CSRD VA
Conflict of Interest Statement
No conflicts of interest, financial or otherwise, are declared by the authors.
References
This article includes 80 references
- Álvarez‐Herms J. Summatory effects of anaerobic exercise and a ‘westernized athletic diet’ on gut dysbiosis and chronic Low‐grade metabolic acidosis. Microorganisms 12, 1138.
- Al Jassim RAM, Scott PT, Trebbin AL, Trott D, Pollitt CC. The genetic diversity of lactic acid producing bacteria in the equine gastrointestinal tract. FEMS Microbiology Letters 248, 75–81.
- Allen KJ, van Erck‐Westergren E, Franklin SH. Exercise testing in the equine athlete. Equine Veterinary Education 28, 89–98.
- Aya V, Flórez A, Perez L, Ramírez JD. Association between physical activity and changes in intestinal microbiota composition: A systematic review. PLoS One 16, e0247039.
- 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 gutjnl‐2016–313627.
- Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, Zhang M, Oh PL, Nehrenberg D, Hua K, Kachman SD, Moriyama EN, Walter J, Peterson DA, Pomp D. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences of the United States of America 107, 18933–18938.
- Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567–590.
- Biddle A, Stewart L, Blanchard J, Leschine S. Untangling the genetic basis of Fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 5, 627–640.
- Biddle AS, Black SJ, Blanchard JL. An in vitro model of the horse gut microbiome enables identification of lactate‐utilizing bacteria that differentially respond to starch induction. PLoS One 8, e77599.
- Bonomini‐Gnutzmann R, Plaza‐Díaz J, Jorquera‐Aguilera C, Rodríguez‐Rodríguez A, Rodríguez‐Rodríguez F. Effect of intensity and duration of exercise on gut microbiota in humans: A systematic review. IJERPH 19, 9518.
- Bressa C, Bailén‐Andrino M, Pérez‐Santiago J, González‐Soltero R, Pérez M, Montalvo‐Lominchar MG, Maté‐Muñoz JL, Domínguez R, Moreno D, Larrosa M. Differences in gut microbiota profile between women with active lifestyle and sedentary women. PLoS One 12, e0171352.
- Bryant MP, Burkey LA. Cultural Methods and some characteristics of some of the more numerous groups of bacteria in the bovine rumen. Journal of Dairy Science 36, 205–217.
- Clarke KR, Owens NJP. A simple and versatile micro‐computer program for the determination of ‘most probable number’. Journal of Microbiological Methods 1, 133–137.
- 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 63, 1913–1920.
- Clauss M, Gérard P, Mosca A, Leclerc M. Interplay between exercise and gut microbiome in the context of human health and performance. Frontiers in Nutrition 8, 637010.
- Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. Journal of Applied Bacteriology 70, 443–459.
- Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28, 1221–1227.
- den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud D‐J, Bakker BM. The role of short‐chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of Lipid Research 54, 2325–2340.
- Deng R, Wang M, Song Y, Shi Y. A bibliometric analysis on the research trend of exercise and the gut microbiome. Microorganisms 11, 903.
- Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI. PICRUSt2 for prediction of metagenome functions. Nature Biotechnology 38, 685–688.
- Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial Flora. Science 308, 1635–1638.
- Escudié F, Auer L, Bernard M, Mariadassou M, Cauquil L, Vidal K, Maman S, Hernandez‐Raquet G, Combes S, Pascal G. FROGS: Find, rapidly, OTUs with galaxy solution. Bioinformatics 34, 1287–1294.
- Estaki M, Pither J, Baumeister P, Little JP, Gill SK, Ghosh S, Ahmadi‐Vand Z, Marsden KR, Gibson DL. Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. Microbiome 4, 42.
- Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, De Vos WM, Cani PD. Cross‐talk between Akkermansia muciniphila and intestinal epithelium controls diet‐induced obesity. Proc Natl Acad Sci USA 110, 9066–9071.
- Fontana F, Longhi G, Tarracchini C, Mancabelli L, Lugli GA, Alessandri G, Turroni F, Milani C, Ventura M. The human gut microbiome of athletes: Metagenomic and metabolic insights. Microbiome 11, 27.
- Frampton J, Murphy KG, Frost G, Chambers ES. Short‐chain fatty acids as potential regulators of skeletal muscle metabolism and function. Nature Metabolism 2, 840–848.
- Froidurot A, Julliand V. Cellulolytic bacteria in the large intestine of mammals. Gut Microbes 14, 2031694.
- Fushimi T, Sato Y. Effect of acetic acid feeding on the circadian changes in glycogen and metabolites of glucose and lipid in liver and skeletal muscle of rats. The British Journal of Nutrition 94, 714–719.
- Garber A, Hastie P, Murray J–A. Factors influencing equine gut microbiota: Current knowledge. Journal of Equine Veterinary Science 88, 102943.
- Grimm P, Combes S, Pascal G, Cauquil L, Julliand V. Dietary composition and yeast/microalgae combination supplementation modulate the microbial ecosystem in the caecum, colon and faeces of horses. The British Journal of Nutrition 123, 372–382.
- Grimm P, Philippeau C, Julliand V. Faecal parameters as biomarkers of the equine hindgut microbial ecosystem under dietary change. Animal 11, 1136–1145.
- Halliwell G, Bryant MP. The cellulolytic activity of pure strains of bacteria from the rumen of cattle. Journal of General Microbiology 32, 441–448.
- Han J‐H, Kim I‐S, Jung S‐H, Lee S‐G, Son H‐Y, Myung C‐S. The effects of propionate and valerate on insulin responsiveness for glucose uptake in 3T3‐L1 adipocytes and C2C12 myotubes via G protein‐coupled receptor 41. PLoS One 9, e95268.
- Han M, Yang K, Yang P, Zhong C, Chen C, Wang S, Lu Q, Ning K. Stratification of athletes' gut microbiota: The multifaceted hubs associated with dietary factors, physical characteristics and performance. Gut Microbes 12, 1–18.
- Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares. Equine Veterinary Journal 15, 371–372.
- Hsu YJ, Chiu CC, Li YP, Huang WC, Huang YT, Huang CC, Chuang HL. Effect of intestinal microbiota on exercise performance in mice. Journal of Strength and Conditioning Research 29, 552–558.
- Hughes RL, Holscher HD. Fueling gut microbes: A review of the interaction between diet, exercise, and the gut microbiota in athletes. Advances in Nutrition 12, 2190–2215.
- Jansson A, Lindberg JE. A forage‐only diet alters the metabolic response of horses in training. Animal 6, 1939–1946.
- Jensen RB, Austbø D, Blache D, Bach Knudsen KE, Tauson A‐H. The effect of feeding barley or hay alone or in combination with molassed sugar beet pulp on the metabolic responses in plasma and caecum of horses. Animal Feed Science and Technology 214, 53–65.
- Jouany J. Volatile fatty acid and alcohol determination in digestive contents, silage juices, bacterial cultures and anaerobic fermentor contents [microbial fermentation, biological liquids, analytic method using gas‐liquid chromatography]. .
- Julliand V, De Fombelle A, Varloud M. Starch digestion in horses: The impact of feed processing. Livestock Science 100, 44–52.
- Julliand V, De Vaux A, Millet L, Fonty G. Identification of Ruminococcus flavefaciens as the predominant cellulolytic bacterial species of the equine cecum. Applied and Environmental Microbiology 65, 3738–3741.
- Karlsson CLJ, Önnerfält J, Xu J, Molin G, Ahrné S, Thorngren‐Jerneck K. The microbiota of the gut in preschool children with Normal and excessive body weight. Obesity 20, 2257–2261.
- Karlsson CP, Jansson A, Essén‐Gustavsson B, Lindberg J‐E. Effect of molassed sugar beet pulp on nutrient utilisation and metabolic parameters during exercise. Equine Veterinary Journal 34, 44–49.
- Kim HJ, Kim YJ, Kim YJ, Baek JH, Kim HS, Kim IY, Seong JK. Microbiota influences host exercise capacity via modulation of skeletal muscle glucose metabolism in mice. Experimental & Molecular Medicine 55, 1820–1830.
- Laroche N, Grimm P, Julliand S, Sorci G. Diet modulates strongyle infection and microbiota in the large intestine of horses. PLoS One 19, e0301920.
- Li C, Li X, Guo R, Ni W, Liu K, Liu Z, Dai J, Xu Y, Abduriyim S, Wu Z, Zeng Y, Lei B, Zhang Y, Wang Y, Zeng W, Zhang Q, Chen C, Qiao J, Liu C, Hu S. Expanded catalogue of metagenome‐assembled genomes reveals resistome characteristics and athletic performance‐associated microbes in horse. Microbiome 11, 7.
- Li Y, Dong J, Xiao H, Zhang S, Wang B, Cui M, Fan S. Gut commensal derived‐valeric acid protects against radiation injuries. Gut Microbes 11, 789–806.
- Liang R, Zhang S, Peng X, Yang W, Xu Y, Wu P, Chen J, Cai Y, Zhou J. Characteristics of the gut microbiota in professional martial arts athletes: A comparison between different competition levels. PLoS One 14, e0226240.
- Liu YR, Du HS, Wu ZZ, Wang C, Liu Q, Guo G, Huo WJ, Zhang YL, Pei CX, Zhang SL. Branched‐chain volatile fatty acids and folic acid accelerated the growth of Holstein dairy calves by stimulating nutrient digestion and rumen metabolism. Animal 14, 1176–1183.
- Lowe SE, Theodorou MK, Trinci AP. Growth and fermentation of an anaerobic rumen fungus on various carbon sources and effect of temperature on development. Applied and Environmental Microbiology 53, 1210–1215.
- Mach N, Midoux C, Leclercq S, Pennarun S, Le Moyec L, Rué O, Robert C, Sallé G, Barrey E. Mining the equine gut metagenome: Poorly‐characterized taxa associated with cardiovascular fitness in endurance athletes. Communications Biology 5, 1032.
- Mailing LJ, Allen JM, Buford TW, Fields CJ, Woods JA. Exercise and the gut microbiome: A review of the evidence, potential mechanisms, and implications for human health. Exercise and Sport Sciences Reviews 47, 75–85.
- Martin A, Lepers R, Vasseur M, Julliand S. Effect of high‐starch or high‐fibre diets on the energy metabolism and physical performance of horses during an 8‐week training period. Frontiers in Physiology 14, 1213032.
- Maruta H, Yoshimura Y, Araki A, Kimoto M, Takahashi Y, Yamashita H. Activation of AMP‐activated protein kinase and stimulation of energy metabolism by acetic acid in L6 myotube cells. PLoS One 11, e0158055.
- McNeil NI. The contribution of the large intestine to energy supplies in man. The American Journal of Clinical Nutrition 39, 338–342.
- Moffett JR, Puthillathu N, Vengilote R, Jaworski DM, Namboodiri AM. Acetate revisited: A key biomolecule at the nexus of metabolism, epigenetics and oncogenesis—Part 1: Acetyl‐CoA, acetogenesis and acyl‐CoA short‐chain synthetases. Frontiers in Physiology 11, 580167.
- Moses FM. Exercise‐Associated Intestinal Ischemia. Current Sports Medicine Reports 4, 91–95.
- National Research Council. Nutrient Requirements of Horses: Sixth Revised Edition. .
- 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. American Journal of Physiology. Endocrinology and Metabolism 317, E158–E171.
- 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. American Journal of Physiology. Endocrinology and Metabolism 316, E956–E966.
- Pan JH, Kim JH, Kim HM, Lee ES, Shin D‐H, Kim S, Shin M, Kim SH, Lee JH, Kim YJ. Acetic acid enhances endurance capacity of exercise‐trained mice by increasing skeletal muscle oxidative properties. Bioscience, Biotechnology, and Biochemistry 79, 1535–1541.
- Park T, Yoon J, Yun Y, Unno T. Comparison of the fecal microbiota with high‐ and low performance race horses. Journal of Animal Science and Technology 66(2), 425–437.
- Pethick DW, Rose RJ, Bryden WL, Gooden JM. Nutrient utilisation by the hindlimb of thoroughbred horses at rest. Equine Veterinary Journal 25, 41–44.
- Poole DC, Erickson HH. Highly Athletic Terrestrial Mammals: Horses and Dogs. Comprehensive Physiology 1–37.
- Powell CD, Dhanoa MS, Garber A, Murray J–AM, López S, Ellis JL, France J. Models based on the Mitscherlich equation for describing typical and atypical gas production profiles obtained from in vitro digestibility studies using equine Faecal inoculum. Animals 10, 308.
- . R: The R Project for Statistical Computing. .
- Roediger WEW. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424–429.
- Sekirov I, Russell SL, Antunes LCM, Finlay BB. Gut microbiota in health and disease. Physiological Reviews 90, 859–904.
- Smith EA, Macfarlane GT. Enumeration of amino acid fermenting bacteria in the human large intestine: Effects of pH and starch on peptide metabolism and dissimilation of amino acids. FEMS Microbiology Ecology 25, 355–368.
- Theodorou MK, Williams BA, Dhanoa MS, McAllan AB, France J. A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology 48, 185–197.
- Van Hall G, Sacchetti M, Rådegran G. Whole body and leg acetate kinetics at rest, during exercise and recovery in humans. The Journal of Physiology 542, 263–272.
- Vermorel M, Martin‐Rosset W. Concepts, scientific bases, structure and validation of the French horse net energy system (UFC). Livestock Production Science 47, 261–275.
- Walshe N, Duggan V, Cabrera‐Rubio R, Crispie F, Cotter P, Feehan O, Mulcahy G. Removal of adult cyathostomins alters faecal microbiota and promotes an inflammatory phenotype in horses. International Journal for Parasitology 49, 489–500.
- Wang SP, Rubio LA, Duncan SH, Donachie GE, Holtrop G, Lo G, Farquharson FM, Wagner J, Parkhill J, Louis P, Walker AW, Flint HJ. Pivotal Roles for pH, Lactate, and Lactate‐Utilizing Bacteria in the Stability of a Human Colonic Microbial Ecosystem. mSystems 5, e00645–20.
- Wedekind KJ, Mansfield HR, Montgomery L. Enumeration and isolation of cellulolytic and hemicellulolytic bacteria from human feces. Applied and Environmental Microbiology 54, 1530–1535.
- Wunderlich G, Bull M, Ross T, Rose M, Chapman B. Understanding the microbial fibre degrading communities & processes in the equine gut. Animal Microbiome 5, 3.
- Xu Y, Zhong F, Zheng X, Lai H‐Y, Wu C, Huang C. Disparity of gut microbiota composition among elite athletes and young adults with different physical activity independent of dietary status: A matching study. Frontiers in Nutrition 9, 843076.
- Yu Z, Morrison M. Improved extraction of PCR‐quality community DNA from digesta and fecal samples. BioTechniques 36, 808–812.
- Zhang Y, Wang C, Peng A, Zhang H, Wang H. Metagenomic insight: Dietary thiamine supplementation promoted the growth of carbohydrate‐associated microorganisms and enzymes in the rumen of Saanen goats fed high‐concentrate diets. Microorganisms 9, 632.
Citations
This article has been cited 0 times.Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists