Understanding the Holobiont: Crosstalk Between Gut Microbiota and Mitochondria During Long Exercise in Horse.
Abstract: Endurance exercise has a dramatic impact on the functionality of mitochondria and on the composition of the intestinal microbiome, but the mechanisms regulating the crosstalk between these two components are still largely unknown. Here, we sampled 20 elite horses before and after an endurance race and used blood transcriptome, blood metabolome and fecal microbiome to describe the gut-mitochondria crosstalk. A subset of mitochondria-related differentially expressed genes involved in pathways such as energy metabolism, oxidative stress and inflammation was discovered and then shown to be associated with butyrate-producing bacteria of the family, especially . The mechanisms involved were not fully understood, but through the action of their metabolites likely acted on the axis and their downstream targets to delay the onset of hypoglycemia, inflammation and extend running time. Our results also suggested that circulating free fatty acids may act not merely as fuel but drive mitochondrial inflammatory responses triggered by the translocation of gut bacterial polysaccharides following endurance. Targeting the gut-mitochondria axis therefore appears to be a potential strategy to enhance athletic performance.
Copyright © 2021 Mach, Moroldo, Rau, Lecardonnel, Le Moyec, Robert and Barrey.
Publication Date: 2021-04-08 PubMed ID: 33898524PubMed Central: PMC8063112DOI: 10.3389/fmolb.2021.656204Google Scholar: Lookup
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Summary
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This study examines the interaction between gut bacteria and mitochondria in horses during endurance exercise. The research uncovers a new understanding of how gut microorganisms and energy-producing cells in the body communicate and influence each other, potentially revealing new ways to enhance athletic performance.
Research Context and Methodology
- In this study, the researchers acknowledged the significant effect of endurance exercise on the functionality of mitochondria, which are the energy powerhouses inside cells, and on the composition of the gut microbiota, the communities of microorganisms living in the intestines.
- The research involved sampling 20 elite horses before and after an endurance race. The researchers analyzed different types of data – the blood transcriptome (the complete set of RNA molecules in blood), blood metabolome (the complete set of metabolites in blood), and fecal microbiome (the microbes in horse feces).
Key Findings
- The researchers identified mitochondria-related genes that showed different levels of activity before and after the endurance exercise. These genes were mainly involved in pathways linked to energy metabolism, oxidative stress, and inflammation.
- These genes were associated with butyrate-producing bacteria of the Lachnospiraceae family, especially Roseburia. These bacteria produce butyrate, a kind of fatty acid that has various health benefits, including anti-inflammatory effects and energy provision for cells lining the colon.
- Through their metabolites, these microbes likely influenced the HIF1-PPAR axis – a pathway involved in regulating oxygen supply and fat metabolism in cells – and their downstream targets. This interaction could help delay the onset of hypoglycemia (low blood sugar) and inflammation, and therefore, extend the time a horse can run.
Additional Implication and Potential Strategy for Improving Performance
- Another significant finding of this study was the prospective role of circulating free fatty acids, not just as simple fuel, but as mediators of inflammatory responses in mitochondria. This reaction could be triggered by the movement of gut bacterial polysaccharides into the bloodstream following endurance exercise.
- The conclusion of the research suggested that targeting the gut-mitochondria axis – the interaction between gut microbiota and mitochondria – might be a promising strategy to enhance athletic performance.
Cite This Article
APA
Mach N, Moroldo M, Rau A, Lecardonnel J, Le Moyec L, Robert C, Barrey E.
(2021).
Understanding the Holobiont: Crosstalk Between Gut Microbiota and Mitochondria During Long Exercise in Horse.
Front Mol Biosci, 8, 656204.
https://doi.org/10.3389/fmolb.2021.656204 Publication
Researcher Affiliations
- Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.
- Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.
- Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.
- BioEcoAgro Joint Research Unit, INRAE, Université de Liège, Université de Lille, Université de Picardie Jules Verne, Estrées-Mons, France.
- Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.
- Université d'Évry Val d'Essonne, Université Paris-Saclay, Évry, France ABI UMR 1313, INRAE, Université Paris-Saclay, AgroParisTech, Jouy-en-Josas, France.
- MCAM UMR7245, CNRS, Muséum National d'Histoire Naturelle, Paris, France.
- Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.
- École Nationale Vétérinaire d'Alfort, Maisons-Alfort, France.
- Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.
Conflict of Interest Statement
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.
References
This article includes 97 references
- Al Amir Dache Z, Otandault A, Tanos R, Pastor B, Meddeb R, Sanchez C, Arena G, Lasorsa L, Bennett A, Grange T, El Messaoudi S, Mazard T, Prevostel C, Thierry AR. Blood contains circulating cell-free respiratory competent mitochondria.. FASEB J 2020 Mar;34(3):3616-3630.
- Bajpai P, Darra A, Agrawal A. Microbe-mitochondrion crosstalk and health: An emerging paradigm.. Mitochondrion 2018 Mar;39:20-25.
- Barrey E, Mucher E, Robert C, Amiot F, Gidrol X. Gene expression profiling in blood cells of endurance horses completing competition or disqualified due to metabolic disorder.. Equine Vet J Suppl 2006 Aug;(36):43-9.
- 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.
- Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pagès F, Trajanoski Z, Galon J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks.. Bioinformatics 2009 Apr 15;25(8):1091-3.
- Blanchet FG, Legendre P, Borcard D. Forward selection of explanatory variables.. Ecology 2008 Sep;89(9):2623-32.
- Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin.. Microbiome 2018 May 17;6(1):90.
- Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis.. ISME J 2017 Dec;11(12):2639-2643.
- Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data.. Nat Methods 2016 Jul;13(7):581-3.
- Calvo SE, Clauser KR, Mootha VK. MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins.. Nucleic Acids Res 2016 Jan 4;44(D1):D1251-7.
- Capomaccio S, Vitulo N, Verini-Supplizi A, Barcaccia G, Albiero A, D'Angelo M, Campagna D, Valle G, Felicetti M, Silvestrelli M, Cappelli K. RNA sequencing of the exercise transcriptome in equine athletes.. PLoS One 2013;8(12):e83504.
- Cardoso SM, Empadinhas N. The Microbiome-Mitochondria Dance in Prodromal Parkinson's Disease.. Front Physiol 2018;9:471.
- Chinnery PF, Hudson G. Mitochondrial genetics.. Br Med Bull 2013;106(1):135-59.
- Clark A, Mach N. The Crosstalk between the Gut Microbiota and Mitochondria during Exercise.. Front Physiol 2017;8:319.
- Clark A, Sallé G, Ballan V, Reigner F, Meynadier A, Cortet J, Koch C, Riou M, Blanchard A, Mach N. Strongyle Infection and Gut Microbiota: Profiling of Resistant and Susceptible Horses Over a Grazing Season.. Front Physiol 2018;9:272.
- Clarke KR, Ainsworth M. A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser. 92, 205–219.
- Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease.. Vet Clin North Am Equine Pract 2018 Apr;34(1):1-12.
- Cottin F, Metayer N, Goachet AG, Julliand V, Slawinski J, Billat V, Barrey E. Oxygen consumption and gait variables of Arabian endurance horses measured during a field exercise test.. Equine Vet J Suppl 2010 Nov;(38):1-5.
- Crisp A, Boschetti C, Perry M, Tunnacliffe A, Micklem G. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes.. Genome Biol 2015 Mar 13;16(1):50.
- Dieterle F, Ross A, Schlotterbeck G, Senn H. Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics.. Anal Chem 2006 Jul 1;78(13):4281-90.
- Dixon P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927.
- Dobashi Y, Miyakawa Y, Yamamoto I, Amao H. Effects of intestinal microflora on superoxide dismutase activity in the mouse cecum.. Exp Anim 2011;60(2):133-9.
- Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product.. Appl Environ Microbiol 2004 Oct;70(10):5810-7.
- Esser C, Ahmadinejad N, Wiegand C, Rotte C, Sebastiani F, Gelius-Dietrich G, Henze K, Kretschmann E, Richly E, Leister D, Bryant D, Steel MA, Lockhart PJ, Penny D, Martin W. A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes.. Mol Biol Evol 2004 Sep;21(9):1643-60.
- Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TM, Comelli EM. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans.. Nutr Diabetes 2014 Jun 30;4(6):e121.
- Fielding CL, Dechant JE. Colic in competing endurance horses presenting to referral centres: 36 cases.. Equine Vet J 2012 Jul;44(4):472-5.
- Franco-Obregón A, Gilbert JA. The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals.. mSystems 2017 May-Jun;2(3).
- Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J. Butyrate improves insulin sensitivity and increases energy expenditure in mice.. Diabetes 2009 Jul;58(7):1509-17.
- Gérard P. Metabolism of cholesterol and bile acids by the gut microbiota.. Pathogens 2013 Dec 30;3(1):14-24.
- Gharechahi J, Vahidi MF, Bahram M, Han JL, Ding XZ, Salekdeh GH. Metagenomic analysis reveals a dynamic microbiome with diversified adaptive functions to utilize high lignocellulosic forages in the cattle rumen.. ISME J 2021 Apr;15(4):1108-1120.
- Goachet AG, Julliand V. Implementation of field cardio-respiratory measurements to assess energy expenditure in Arabian endurance horses.. Animal 2015 May;9(5):787-92.
- Gruber J, Kennedy BK. Microbiome and Longevity: Gut Microbes Send Signals to Host Mitochondria.. Cell 2017 Jun 15;169(7):1168-1169.
- Gunn H M. Muscle, bone and fat proportions and muscle distribution of thoroughbreds and other horses. in International conference on equine exercise physiology. Editors Gillespie J. R., Robinson N. E. (Davis, CA: ICEEP Publications; ), 253–264.
- Han B, Sivaramakrishnan P, Lin CJ, Neve IAA, He J, Tay LWR, Sowa JN, Sizovs A, Du G, Wang J, Herman C, Wang MC. Microbial Genetic Composition Tunes Host Longevity.. Cell 2017 Jun 15;169(7):1249-1262.e13.
- Hawley JA, Lundby C, Cotter JD, Burke LM. Maximizing Cellular Adaptation to Endurance Exercise in Skeletal Muscle.. Cell Metab 2018 May 1;27(5):962-976.
- Hawley JA. Microbiota and muscle highway - two way traffic.. Nat Rev Endocrinol 2020 Feb;16(2):71-72.
- Henagan TM, Stefanska B, Fang Z, Navard AM, Ye J, Lenard NR, Devarshi PP. Sodium butyrate epigenetically modulates high-fat diet-induced skeletal muscle mitochondrial adaptation, obesity and insulin resistance through nucleosome positioning.. Br J Pharmacol 2015 Jun;172(11):2782-98.
- Hood DA, Uguccioni G, Vainshtein A, D'souza D. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle: implications for health and disease.. Compr Physiol 2011 Jul;1(3):1119-34.
- Jackson DN, Theiss AL. Gut bacteria signaling to mitochondria in intestinal inflammation and cancer.. Gut Microbes 2020 May 3;11(3):285-304.
- Jang HJ, Kim DM, Kim KB, Park JW, Choi JY, Oh JH, Song KD, Kim S, Cho BW. Analysis of metabolomic patterns in thoroughbreds before and after exercise.. Asian-Australas J Anim Sci 2017 Nov;30(11):1633-1642.
- Janouškovec J, Tikhonenkov DV, Burki F, Howe AT, Rohwer FL, Mylnikov AP, Keeling PJ. A New Lineage of Eukaryotes Illuminates Early Mitochondrial Genome Reduction.. Curr Biol 2017 Dec 4;27(23):3717-3724.e5.
- Neish AS, Jones RM. Redox signaling mediates symbiosis between the gut microbiota and the intestine.. Gut Microbes 2014 Mar-Apr;5(2):250-3.
- Karlsson FH, Tremaroli V, Nookaew I, Bergström G, Behre CJ, Fagerberg B, Nielsen J, Bäckhed F. Gut metagenome in European women with normal, impaired and diabetic glucose control.. Nature 2013 Jun 6;498(7452):99-103.
- Kauffmann A, Gentleman R, Huber W. arrayQualityMetrics--a bioconductor package for quality assessment of microarray data.. Bioinformatics 2009 Feb 1;25(3):415-6.
- Kauter A, Epping L, Semmler T, Antao EM, Kannapin D, Stoeckle SD, Gehlen H, Lübke-Becker A, Günther S, Wieler LH, Walther B. The gut microbiome of horses: current research on equine enteral microbiota and future perspectives.. Anim Microbiome 2019 Nov 13;1(1):14.
- 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.
- Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis.. BMC Bioinformatics 2008 Dec 29;9:559.
- Le Moyec L, Robert C, Triba MN, Billat VL, Mata X, Schibler L, Barrey E. Protein catabolism and high lipid metabolism associated with long-distance exercise are revealed by plasma NMR metabolomics in endurance horses.. PLoS One 2014;9(3):e90730.
- Le Moyec L, Robert C, Triba MN, Bouchemal N, Mach N, Rivière J, Zalachas-Rebours E, Barrey E. A First Step Toward Unraveling the Energy Metabolism in Endurance Horses: Comparison of Plasma Nuclear Magnetic Resonance Metabolomic Profiles Before and After Different Endurance Race Distances.. Front Mol Biosci 2019;6:45.
- Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18.
- Mach N, Berri M, Estellé J, Levenez F, Lemonnier G, Denis C, Leplat JJ, Chevaleyre C, Billon Y, Doré J, Rogel-Gaillard C, Lepage P. Early-life establishment of the swine gut microbiome and impact on host phenotypes.. Environ Microbiol Rep 2015 Jun;7(3):554-69.
- Mach N, Foury A, Kittelmann S, Reigner F, Moroldo M, Ballester M, Esquerré D, Rivière J, Sallé G, Gérard P, Moisan MP, Lansade L. The Effects of Weaning Methods on Gut Microbiota Composition and Horse Physiology.. Front Physiol 2017;8:535.
- Mach N, Fuster-Botella D. Endurance exercise and gut microbiota: A review.. J Sport Health Sci 2017 Jun;6(2):179-197.
- Mach N, Plancade S, Pacholewska A, Lecardonnel J, Rivière J, Moroldo M, Vaiman A, Morgenthaler C, Beinat M, Nevot A, Robert C, Barrey E. Integrated mRNA and miRNA expression profiling in blood reveals candidate biomarkers associated with endurance exercise in the horse.. Sci Rep 2016 Mar 10;6:22932.
- Mach N, Ramayo-Caldas Y, Clark A, Moroldo M, Robert C, Barrey E, López JM, Le Moyec L. Understanding the response to endurance exercise using a systems biology approach: combining blood metabolomics, transcriptomics and miRNomics in horses.. BMC Genomics 2017 Feb 17;18(1):187.
- Mach N, Ruet A, Clark A, Bars-Cortina D, Ramayo-Caldas Y, Crisci E, Pennarun S, Dhorne-Pollet S, Foury A, Moisan MP, Lansade L. Priming for welfare: gut microbiota is associated with equitation conditions and behavior in horse athletes.. Sci Rep 2020 May 20;10(1):8311.
- Maier UG, Zauner S, Woehle C, Bolte K, Hempel F, Allen JF, Martin WF. Massively convergent evolution for ribosomal protein gene content in plastid and mitochondrial genomes.. Genome Biol Evol 2013;5(12):2318-29.
- Massacci FR, Clark A, Ruet A, Lansade L, Costa M, Mach N. Inter-breed diversity and temporal dynamics of the faecal microbiota in healthy horses.. J Anim Breed Genet 2020 Jan;137(1):103-120.
- McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8(4):e61217.
- McMurdie PJ, Holmes S. Phyloseq: a bioconductor package for handling and analysis of high-throughput phylogenetic sequence data.. Pac Symp Biocomput 2012;:235-46.
- Mohr S, Liew CC. The peripheral-blood transcriptome: new insights into disease and risk assessment.. Trends Mol Med 2007 Oct;13(10):422-32.
- Mollica MP, Mattace Raso G, Cavaliere G, Trinchese G, De Filippo C, Aceto S, Prisco M, Pirozzi C, Di Guida F, Lama A, Crispino M, Tronino D, Di Vaio P, Berni Canani R, Calignano A, Meli R. Butyrate Regulates Liver Mitochondrial Function, Efficiency, and Dynamics in Insulin-Resistant Obese Mice.. Diabetes 2017 May;66(5):1405-1418.
- Mottawea W, Chiang CK, Mühlbauer M, Starr AE, Butcher J, Abujamel T, Deeke SA, Brandel A, Zhou H, Shokralla S, Hajibabaei M, Singleton R, Benchimol EI, Jobin C, Mack DR, Figeys D, Stintzi A. Altered intestinal microbiota-host mitochondria crosstalk in new onset Crohn's disease.. Nat Commun 2016 Nov 23;7:13419.
- 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.
- 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.
- Oksanen J, Blanchet F G, Kindt R, Minchin P R, O’Hara R B, Simpson G L. Package ‘vegan’: a community ecology package. 260.
- Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK. A mitochondrial protein compendium elucidates complex I disease biology.. Cell 2008 Jul 11;134(1):112-23.
- Pfanner N, Warscheid B, Wiedemann N. Mitochondrial proteins: from biogenesis to functional networks.. Nat Rev Mol Cell Biol 2019 May;20(5):267-284.
- Plancade S, Clark A, Philippe C, Helbling JC, Moisan MP, Esquerré D, Le Moyec L, Robert C, Barrey E, Mach N. Unraveling the effects of the gut microbiota composition and function on horse endurance physiology.. Sci Rep 2019 Jul 3;9(1):9620.
- Qi B, Han M. Microbial Siderophore Enterobactin Promotes Mitochondrial Iron Uptake and Development of the Host via Interaction with ATP Synthase.. Cell 2018 Oct 4;175(2):571-582.e11.
- Rapoport BI. Metabolic factors limiting performance in marathon runners.. PLoS Comput Biol 2010 Oct 21;6(10):e1000960.
- Richter-Dennerlein R, Oeljeklaus S, Lorenzi I, Ronsör C, Bareth B, Schendzielorz AB, Wang C, Warscheid B, Rehling P, Dennerlein S. Mitochondrial Protein Synthesis Adapts to Influx of Nuclear-Encoded Protein.. Cell 2016 Oct 6;167(2):471-483.e10.
- Rodríguez-Carrio J, Salazar N, Margolles A, González S, Gueimonde M, de Los Reyes-Gavilán CG, Suárez A. Free Fatty Acids Profiles Are Related to Gut Microbiota Signatures and Short-Chain Fatty Acids.. Front Immunol 2017;8:823.
- Rohart F, Gautier B, Singh A, Lê Cao KA. mixOmics: An R package for 'omics feature selection and multiple data integration.. PLoS Comput Biol 2017 Nov;13(11):e1005752.
- Ropka-Molik K, Stefaniuk-Szmukier M, Żukowski K, Piórkowska K, Gurgul A, Bugno-Poniewierska M. Transcriptome profiling of Arabian horse blood during training regimens.. BMC Genet 2017 Apr 5;18(1):31.
- Ruiz E, Penrose HM, Heller S, Nakhoul H, Baddoo M, Flemington EF, Kandil E, Savkovic SD. Bacterial TLR4 and NOD2 signaling linked to reduced mitochondrial energy function in active inflammatory bowel disease.. Gut Microbes 2020 May 3;11(3):350-363.
- Saint-Georges-Chaumet Y, Attaf D, Pelletier E, Edeas M. Targeting microbiota-mitochondria inter-talk: Microbiota control mitochondria metabolism.. Cell Mol Biol (Noisy-le-grand) 2015 Sep 26;61(4):121-4.
- Saint-Georges-Chaumet Y, Edeas M. Microbiota-mitochondria inter-talk: consequence for microbiota-host interaction.. Pathog Dis 2016 Feb;74(1):ftv096.
- 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.
- Scott JM, Esch BT, Shave R, Warburton DE, Gaze D, George K. Cardiovascular consequences of completing a 160-km ultramarathon.. Med Sci Sports Exerc 2009 Jan;41(1):26-34.
- Seok S, Fu T, Choi SE, Li Y, Zhu R, Kumar S, Sun X, Yoon G, Kang Y, Zhong W, Ma J, Kemper B, Kemper JK. Transcriptional regulation of autophagy by an FXR-CREB axis.. Nature 2014 Dec 4;516(7529):108-11.
- Singh A, Shannon CP, Gautier B, Rohart F, Vacher M, Tebbutt SJ, Lê Cao KA. DIABLO: an integrative approach for identifying key molecular drivers from multi-omics assays.. Bioinformatics 2019 Sep 1;35(17):3055-3062.
- Smith AC, Robinson AJ. MitoMiner v4.0: an updated database of mitochondrial localization evidence, phenotypes and diseases.. Nucleic Acids Res 2019 Jan 8;47(D1):D1225-D1228.
- Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments.. Stat Appl Genet Mol Biol 2004;3:Article3.
- Smyth GK, Michaud J, Scott HS. Use of within-array replicate spots for assessing differential expression in microarray experiments.. Bioinformatics 2005 May 1;21(9):2067-75.
- Song X, Hu W, Yu H, Wang H, Zhao Y, Korngold R, Zhao Y. Existence of Circulating Mitochondria in Human and Animal Peripheral Blood.. Int J Mol Sci 2020 Mar 19;21(6).
- Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. The Controversial Role of Human Gut Lachnospiraceae.. Microorganisms 2020 Apr 15;8(4).
- van der Kolk JH, Thomas S, Mach N, Ramseyer A, Burger D, Gerber V, Nuoffer JM. Serum acylcarnitine profile in endurance horses with and without metabolic dysfunction.. Vet J 2020 Jan;255:105419.
- Vezza T, Abad-Jiménez Z, Marti-Cabrera M, Rocha M, Víctor VM. Microbiota-Mitochondria Inter-Talk: A Potential Therapeutic Strategy in Obesity and Type 2 Diabetes.. Antioxidants (Basel) 2020 Sep 10;9(9).
- Vital M, Gao J, Rizzo M, Harrison T, Tiedje JM. Diet is a major factor governing the fecal butyrate-producing community structure across Mammalia, Aves and Reptilia.. ISME J 2015 Mar 17;9(4):832-43.
- Votion DM, Gnaiger E, Lemieux H, Mouithys-Mickalad A, Serteyn D. Physical fitness and mitochondrial respiratory capacity in horse skeletal muscle.. PLoS One 2012;7(4):e34890.
- Wang F, Wang K, Xu W, Zhao S, Ye D, Wang Y, Xu Y, Zhou L, Chu Y, Zhang C, Qin X, Yang P, Yu H. SIRT5 Desuccinylates and Activates Pyruvate Kinase M2 to Block Macrophage IL-1β Production and to Prevent DSS-Induced Colitis in Mice.. Cell Rep 2017 Jun 13;19(11):2331-2344.
- Wong ML, Inserra A, Lewis MD, Mastronardi CA, Leong L, Choo J, Kentish S, Xie P, Morrison M, Wesselingh SL, Rogers GB, Licinio J. Inflammasome signaling affects anxiety- and depressive-like behavior and gut microbiome composition.. Mol Psychiatry 2016 Jun;21(6):797-805.
- Wu Z, Huang X, Feng Y, Handschin C, Feng Y, Gullicksen PS, Bare O, Labow M, Spiegelman B, Stevenson SC. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells.. Proc Natl Acad Sci U S A 2006 Sep 26;103(39):14379-84.
- Yardeni T, Tanes CE, Bittinger K, Mattei LM, Schaefer PM, Singh LN, Wu GD, Murdock DG, Wallace DC. Host mitochondria influence gut microbiome diversity: A role for ROS.. Sci Signal 2019 Jul 2;12(588).
- Zhang Y, Kumarasamy S, Mell B, Cheng X, Morgan EE, Britton SL, Vijay-Kumar M, Koch LG, Joe B. Vertical selection for nuclear and mitochondrial genomes shapes gut microbiota and modifies risks for complex diseases.. Physiol Genomics 2020 Jan 1;52(1):1-14.
- Zheng C, Zhang S, Ragg S, Raftery D, Vitek O. Identification and quantification of metabolites in (1)H NMR spectra by Bayesian model selection.. Bioinformatics 2011 Jun 15;27(12):1637-44.
Citations
This article has been cited 9 times.- Tuniyazi M, Wang W, Zhang N. A Systematic Review of Current Applications of Fecal Microbiota Transplantation in Horses.. Vet Sci 2023 Apr 13;10(4).
- 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 2023 Jan 12;11(1):7.
- Chaucheyras-Durand F, Sacy A, Karges K, Apper E. Gastro-Intestinal Microbiota in Equines and Its Role in Health and Disease: The Black Box Opens.. Microorganisms 2022 Dec 19;10(12).
- 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.. Commun Biol 2022 Oct 3;5(1):1032.
- Belhaj MR, Lawler NG, Hawley JA, Broadhurst DI, Hoffman NJ, Reinke SN. Metabolomics reveals mouse plasma metabolite responses to acute exercise and effects of disrupting AMPK-glycogen interactions.. Front Mol Biosci 2022;9:957549.
- Burtscher J, Ticinesi A, Millet GP, Burtscher M, Strasser B. Exercise-microbiota interactions in aging-related sarcopenia.. J Cachexia Sarcopenia Muscle 2022 Apr;13(2):775-780.
- de Meeûs d'Argenteuil C, Boshuizen B, Vidal Moreno de Vega C, Leybaert L, de Maré L, Goethals K, De Spiegelaere W, Oosterlinck M, Delesalle C. Comparison of Shifts in Skeletal Muscle Plasticity Parameters in Horses in Three Different Muscles, in Answer to 8 Weeks of Harness Training.. Front Vet Sci 2021;8:718866.
- Zhu Y, Wang X, Liu B, Yi Z, Zhao Y, Deng L, Holyoak R, Li J. The Effect of Ryegrass Silage Feeding on Equine Fecal Microbiota and Blood Metabolite Profile.. Front Microbiol 2021;12:715709.
- Mach N, Baranowski E, Nouvel LX, Citti C. The Airway Pathobiome in Complex Respiratory Diseases: A Perspective in Domestic Animals.. Front Cell Infect Microbiol 2021;11:583600.
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