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The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level
Open accessAbstract
Objective: It is evident that the gut microbiota and factors that influence its composition and activity effect human metabolic, immunological and developmental processes. We previously reported that extreme physical activity with associated dietary adaptations, such as that pursued by professional athletes, is associated with changes in faecal microbial diversity and composition relative to that of individuals with a more sedentary lifestyle. Here we address the impact of these factors on the functionality/metabolic activity of the microbiota which reveals even greater separation between exercise and a more sedentary state. Design: Metabolic phenotyping and functional metagenomic analysis of the gut microbiome of professional international rugby union players (n=40) and controls (n=46) was carried out and results were correlated with lifestyle parameters and clinical measurements (eg, dietary habit and serum creatine kinase, respectively). Results: Athletes had relative increases in pathways (eg, amino acid and antibiotic biosynthesis and carbohydrate metabolism) and faecal metabolites (eg, microbial produced short-chain fatty acids (SCFAs) acetate, propionate and butyrate) associated with enhanced muscle turnover (fitness) and overall health when compared with control groups. Conclusions: Differences in faecal microbiota between athletes and sedentary controls show even greater separation at the metagenomic and metabolomic than at compositional levels and provide added insight into the diet–exercise–gut microbiota paradigm.
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“The impact of the athletes' increased protein intake compared to both control groups was evident in the metabolomic phenotyping results.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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“of the total 19,300 pathways, 98 were significantly altered between the three cohorts (p < 0.05)”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Functional structure of the enteric microbiome correlates with athletic state
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“Furthermore, athletes have an enriched profile of SCFAs, previously associated with numerous health benefits and a lean phenotype.[33][34][35]”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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“The relative abundances of pathways related to fundamental metabolic function-amino acid biosynthesis, vitamin biosynthesis, and lipid biosynthesis-were higher on average within the high BMI control group when compared to the athlete group.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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“Notably, from a functional perspective, the microbiota of the low BMI group was more similar to the athletes.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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“Comparing athletes to both high and low BMI controls, a greater number of pathways correlating to specific macronutrients with the controls suggests a shift in the dynamics of these varied metabolic functions.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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“SCFAs were also correlated with pathway relative abundances, with all SCFAs associating with considerably more pathways in the athletes versus the controls (Fig. 4C).”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Correlating metabonomic and metagenomic results
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“Beta-alanine betaine was higher in both faecal and urine samples of athletes.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Distinct differences between host and microbial metabolites in athletes and controls
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“with the high BMI control group having the lowest average abundance scores across 31 metabolic pathway categories (the exceptions being Vitamin Biosynthesis (VB), Lipid Biosynthesis (LB), and Amino Acid Biosynthesis (AAB) categories).”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Functional structure of the enteric microbiome correlates with athletic state
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“The athlete group had the highest mean abundance across 29 of the 34 metabolic categories”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Functional structure of the enteric microbiome correlates with athletic state
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“Athletes' 1 H-NMR metabolic phenotypes were characterised by higher levels of trimethylamine-N-oxide (TMAO), L-carnitine, dimethylglycine, O-acetyl carnitine, proline betaine, creatinine, acetoacetate, 3-hydroxyisovaleric acid, acetone, N-methylnicotinate, N-methylnicotinamide, phenylacetylglutamine (PAG) and 3-methylhistidine in urine samples and higher levels of propionate, acetate, butyrate, tr”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Distinct differences between host and microbial metabolites in athletes and controls
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In the paper
“Athletes have an increased abundance of pathways that-giving an equivalent amount of expression activity-could be exploited by the host for potential health benefit, including biosynthesis of organic cofactors and antibiotics, as well as carbohydrate degradation and secondary metabolite metabolism compared to both control groups.[32]”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
What the sources say
- Not checked yetcites [32] source
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In the paper
“Separation according to group membership was further illustrated through Principal Coordinate Analysis (PCoA), with statistical support of the significant separation between the athletes and both control groups (p < 0.05) (Fig. 2B).”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Functional structure of the enteric microbiome correlates with athletic state
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“Roseburia was positively correlated with acetate (p = 0.004) and butyrate (p = 0.018) while Family XIII Incertae Sedis was positively correlated with isobutyrate (p < 0.001), isovaleric acid (p < 0.001) and valeric acid (p = 0.008)”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Correlating metabonomic and metagenomic results
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“Furthermore, concentrations of propionate strongly correlated to protein intake while butyrate was shown to have a strong association with intake of dietary fibre (Supplementary Table 6).”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Distinct differences between host and microbial metabolites in athletes and controls
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“Likewise, the CV-OPLS-DA models comparing faecal samples, although weaker than the urine models, reveal significant differences between athletes and controls by 1 H-NMR analysis (R 2 Y=0.86, Q 2 Y=0.52, Fig. 2D) and HILIC UPLC-MS positive mode analysis (R 2 Y=0.65, Q 2 Y=0.34, Supplementary Fig 2D).”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Distinct differences between host and microbial metabolites in athletes and controls
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“Subsequently, large-scale functional dissimilarity between athletes and controls was determined and distinct patterns of pathway composition between groups were revealed”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Functional structure of the enteric microbiome correlates with athletic state
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In the paper
“SCFA levels in faeces measured by targeted GC-MS showed significantly higher levels of acetate (p < 0.001), propionate (p < 0.001), butyrate (p < 0.001) and valerate (p = 0.011) in athletes relative to controls.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Distinct differences between host and microbial metabolites in athletes and controls
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In the paper
“By-products of dietary protein metabolism (mostly by microbes) including TMAO, carnitines, trimethylamine, 3-Carboxy-4-methyl-5-propyl-2-furanpropionic acid, and 3-hydroxy-isovaleric acid are all elevated in the athlete cohort.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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In the paper
“Each group was represented by distinct association profiles of the correlation between clinical measurements and metagenomic pathways.Dietary factors, sugars and other carbohydrates, as well as energy intake, provide the majority of the correlation for the control groups whereas the athlete group was predominantly correlated with CK, total bilirubin, and total energy intake.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > [CfB], and Energy Metabolism [EM]) (Supplementary table 2).
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In the paper
“Similarly to these populations, the athletes' diet contained a significantly greater proportion of fish.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Two distinct blocks of proportionately discriminant correlations were observed with isobutyric and isovaleric acids, which were more abundant in the athletes while acetic and butyric acids were more proportionately abundant in controls.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Correlating metabonomic and metagenomic results
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In the paper
“Athletes were further characterised by lower levels of glycerate, allantoin and succinate and lower levels of glycine and tyrosine relative to controls in urine and faecal samples, respectively (Supplementary Table 3).”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Distinct differences between host and microbial metabolites in athletes and controls
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In the paper
“The same clusters are observed when correlating with individual taxa, in support of previously observed links between SCFAs and numerous metabolic benefits and a lean phenotype.[33][34][35]”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
What the sources say
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Diversity measures are statistically significant between low BMI and athletes (p < 0.049), with statistical significance between all groups (Kruskal Wallis p < 0.05).”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Additional information
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In the paper
“Furthermore, PAG positively correlates with the genus Erysipelotrichaceae Incertae Sedis, which we have previously noted to be present in relatively higher proportions in the athlete group compared to both control groups.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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In the paper
“Heat map of bacterial taxa (family, genus, and species level) that correlate with faecal short-chain fatty acid levels using Spearman's correlation.”
- Also stated in: § Additional information · plain
“All taxa shown had a correlation p-value < 0.01.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Additional information
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- Also stated in: § Additional information · plain
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In the paper
“Within the SCFAs, two distinct clusters were observed; acetic acid, propionic acid and butyric acid correlate with dietary contributors (fibre and protein), while isobutyric acid, isovaleric acid and valeric acid correlate with microbial diversity.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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In the paper
“associated with enhanced muscle turnover (fitness) and overall health when compared to control groups.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Results
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In the paper
“Elevated TMAO has been observed in patients with cardiovascular disease and atherosclerosis, highlighting a potential downside to increased protein intake.[15-17,22, 37]”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
What the sources say
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“On the contrary, the athlete microbiome presents a functional capacity that is primed for tissue repair and to harness energy from the diet with increased capacity for carbohydrate, cell structure and nucleotide biosynthesis, reflecting the significant energy demands and high cell-turnover evident in elite sport.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
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In the paper
“Participants made no report of gastrointestinal (GI) distress or alterations of GI transit time throughout the course of the initial study.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > RESULTS
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In the paper
“Approval for this study was granted by the Cork Clinical Research Ethics Committee.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Study population
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In the paper
“3-hydroxy-isovaleric acid (potentially from egg consumption) which has been demonstrated to have efficacy for inhibiting muscle wasting when used in conjunction of physical exercise.[40]”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
What the sources say
- Not checked yetcites [40] Stratton, 2006, Lymphocyte propionyl-CoA carboxylase and its activation by biotin are sensitive indicators of marginal biotin deficiency in humans, Am J Clin Nutr source
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In the paper
“All presented p values were corrected for multiple comparisons using the Benjamini-Hochberg False Discovery Rate (pFDR) method.[47]”
- Also stated in: § Metabolic profiling · plain
“P-values were adjusted for multiple testing using the Benjamini-Hochberg False Discovery Rate (pFDR) method.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Metagenomic statistical and bioinformatic analysis
What the sources say
- Not checked yetcites [47] source
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- Also stated in: § Metabolic profiling · plain
In the paper
“It is notable that PAG-a microbial conversion product of phenylalanine-has been associated with a lean phenotype, and is increased in the athletes.[42]”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
What the sources say
- Not checked yetcites [42] source
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In the paper
“The compound is also commonly used as a supplement by athletes to increase exercise-induced gains in muscle size, muscle strength, and lean body mass, reduce exercise-induced muscle damage, and speed recovery from highintensity exercise.[41]”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
What the sources say
- Not checked yetcites [41] source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
The paper relies on this without support.
The control participants are representative of a more sedentary lifestyle than the athletes.
“The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“These findings support the role of A muciniphila in metabolic regulation.”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [110]
In the citing paper
“For example, levels of SCFAs were significantly higher in athletes compared with controls,”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [110]
In the citing paper
“Among the individual species that differed between athletes and controls, A muciniphila was found to be enriched by 16s rRNA and metagenomic sequencing analyses, as well as in the metabolic pathway analysis.”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [110]
In the citing paper
“The athletes were found to have a more diverse gut microbiome than the controls.”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [110]
In the citing paper
“A high-fiber diet and exercise are associated with increased diversity of the gut microbiota and enrichment of short chain fatty acids (SCFAs), both of which have been implicated in improved survival following treatment with ICB”
From Hallmarks of response, resistance, and toxicity to immune checkpoint blockade (2021) · cites this paper as Barton et al., 2018
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In the paper
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > Distinct differences between host and microbial metabolites in athletes and controls
“Levels of glutamine, 7methylxanthine, imidazoleacetic acid, isoquinoline / quinolone were lower in athletes' urinary samples relative to controls.”
§ The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level > DISCUSSION
“Metabolites derived from vitamins and recovery supplements common in professional sports, including glutamine, lysine, 4-pyridoxic acid, and nicotinamide, are also raised in the athlete group.”
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Metadata
- Authors
- Barton, W., Penney, N. C., Cronin, O., Garcia-Perez, I., Molloy, M. G., Holmes, E., Shanahan, F., Cotter, P. D., & O'Sullivan, O.
- Affiliations
- Teagasc - The Irish Agriculture and Food Development Authority (IE)
- Imperial College London (GB)
- National University of Ireland (IE)
- Section of Biomolecular Medicine, Division of Computational Systems Medicine, Department of Surgery and Cancer, Imperial College London, London, UK
- Alimentary Pharmabiotic Centre Microbiome Institute, University College Cork, National University of Ireland, Cork, Ireland
- Corresponding author
- Shanahan, Fergus
- ORCID
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2017-03-30
- Volume
- 67
- Issue
- 4
- Pages
- 625-633
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- OpenAlex
- W2597526148
- Cited by
- 647
- References
- 0
- Citations by year
- 2026: 73 · 2025: 73 · 2024: 79 · 2023: 84 · 2022: 92 · 2021: 89 · 2020: 56 · 2019: 61 · 2018: 26 · 2017: 12
- FWCI
- 17.30
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Locations
- Gut (publishedVersion)
- PubMed (publishedVersion)
- Cork Open Research Archive (University College Cork, Ireland) (submittedVersion)
- Arrow@dit (Dublin Institute of Technology) (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Spiral (Imperial College London) (submittedVersion)
- Funders
- Science Foundation Ireland (11/PI/1137, 13/SIRG/2160, SFI/12/RC/2273)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- gut microbiota, professional athletes, rugby union players, physical activity, sedentary lifestyle, microbial metabolic functions, short-chain fatty acids, fecal metabolites, amino acid biosynthesis, carbohydrate metabolism, antibiotic biosynthesis, serum creatine kinase, functional metagenomics
- MeSH terms
- Gastrointestinal Microbiome, Feces, Feeding Behavior, Female, Humans, Male, Exercise, Body Mass Index, Case-Control Studies, Young Adult, Athletes
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