Cited by 647Gut microbiota and healthProbiotics and Fermented FoodsGastrointestinal motility and disorders

The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level

Open access
Barton, Wiley, Penney, Nicholas C, Cronin, Owen, Garcia-Perez, Isabel, Molloy, Michael G, Holmes, Elaine, Shanahan, Fergus, Cotter, Paul D +1 more·2018·Gut

Abstract

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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Crossref · 10.1136/gutjnl-2016-313627

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Claims the paper makes

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  • Findingown data

    The impact of the athletes' increased protein intake compared to both control groups was evident in the metabolomic phenotyping results.

    “The impact of the athletes' increased protein intake compared to both control groups was evident in the metabolomic phenotyping results.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Of 19,300 taxonomically linked metabolic pathways, 98 were significantly altered between the three cohorts (p < 0.05).

    “of the total 19,300 pathways, 98 were significantly altered between the three cohorts (p < 0.05)”
    Quote in the paperSubstantial claim
  • Findingcitation

    Athletes have an enriched profile of SCFAs, previously associated with numerous health benefits and a lean phenotype.

    “Furthermore, athletes have an enriched profile of SCFAs, previously associated with numerous health benefits and a lean phenotype.[33][34][35]”
    Quote in the paperSubstantial claim0 of 3 sources checked
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  • Findingown data

    The relative abundances of pathways related to 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 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.”
    Quote in the paperSubstantial claim
  • Findingown data

    From a functional perspective, the microbiota of the low BMI group was more similar to the athletes.

    “Notably, from a functional perspective, the microbiota of the low BMI group was more similar to the athletes.”
    Quote in the paperSubstantial claim
  • May combine two claims. 21
  • Classified as probably not a substantial claim. 8
  • The quote only partly states this claim. 1
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    Findingown data

    Athletes' 1H-NMR metabolic phenotypes were characterised by higher levels of TMAO, L-carnitine, dimethylglycine, O-acetyl carnitine, proline betaine, creatinine, acetoacetate, 3-hydroxyisovaleric acid, acetone, N-methylnicotinate, N-methylnicotinamide, PAG, and 3-methylhistidine in urine, and higher levels of propionate, acetate, butyrate, TMA, lysine, and methylamine in faecal samples, relative t

    “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”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingcitation

    Athletes have an increased abundance of pathways that 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.

    “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]”
    Quote in the paperSubstantial claim0 of 1 sources checked
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    Findingown data

    Separation according to group membership was illustrated through PCoA, with significant separation between athletes and both control groups (p < 0.05).

    “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).”
    Quote in the paperSubstantial claim
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    Findingown data

    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).

    “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)”
    Quote in the paperSubstantial claim
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    Findingown data

    Concentrations of propionate strongly correlated to protein intake while butyrate had a strong association with intake of dietary fibre.

    “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).”
    Quote in the paperNot a substantial claim
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    Findingown data

    CV-OPLS-DA models comparing faecal samples reveal significant differences between athletes and controls by 1H-NMR and HILIC UPLC-MS positive mode, although weaker than urine models.

    “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).”
    Quote in the paperSubstantial claim
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    Findingown data

    Large-scale functional dissimilarity between athletes and controls was determined and distinct patterns of pathway composition between groups were revealed.

    “Subsequently, large-scale functional dissimilarity between athletes and controls was determined and distinct patterns of pathway composition between groups were revealed”
    Quote in the paperSubstantial claim
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    Findingown data

    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.

    “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.”
    Quote in the paperSubstantial claim
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    Findingown data

    By-products of dietary protein metabolism including TMAO, carnitines, trimethylamine, CMPF, and 3-hydroxy-isovaleric acid are all elevated in the athlete cohort.

    “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.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Each group was represented by distinct association profiles between clinical measurements and metagenomic pathways; dietary factors provided majority of correlation for control groups whereas athlete group was predominantly correlated with CK, total bilirubin, and total energy intake.

    “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.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    The athletes' diet contained a significantly greater proportion of fish.

    “Similarly to these populations, the athletes' diet contained a significantly greater proportion of fish.”
    Quote in the paperNot a substantial claim
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    Findingown data

    Two distinct blocks of proportionately discriminant correlations were observed with isobutyric and isovaleric acids, which were more abundant in athletes, while acetic and butyric acids were more proportionately abundant in controls.

    “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.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Athletes had lower levels of glycerate, allantoin, and succinate in urine and lower levels of glycine and tyrosine in faecal samples relative to controls.

    “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).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingcitation

    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.

    “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]”
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  • May combine two claims.

    Findingown data

    Pathway diversity differs significantly between low-BMI controls and athletes (p<0.049), and diversity differs significantly across all three groups (Kruskal-Wallis p<0.05).

    “Diversity measures are statistically significant between low BMI and athletes (p < 0.049), with statistical significance between all groups (Kruskal Wallis p < 0.05).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    PAG positively correlates with the genus Erysipelotrichaceae Incertae Sedis, which the authors have previously noted to be present in relatively higher proportions in the athlete group compared to both control groups.

    “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.”
    Quote in the paperNot a substantial claim
  • The quote only partly states this claim.

    Findingown data

    Bacterial taxa at family, genus and species level correlate with faecal short-chain fatty acid levels (Spearman's correlation, p<0.01).

    “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.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Within 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.

    “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.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    These increases are associated with enhanced muscle turnover (fitness) and overall health.

    “associated with enhanced muscle turnover (fitness) and overall health when compared to control groups.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Elevated TMAO has been observed in patients with cardiovascular disease and atherosclerosis, highlighting a potential downside to increased protein intake.

    “Elevated TMAO has been observed in patients with cardiovascular disease and atherosclerosis, highlighting a potential downside to increased protein intake.[15-17,22, 37]”
    Quote in the paperNot a substantial claim0 of 5 sources checked
    • cites [15] source

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    • cites [17] Tang, 2017, Microbiome, trimethylamine N-oxide, and cardiometabolic disease, Transl Res source

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    • cites [22] source

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    • cites [37] source

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  • May combine two claims.

    Interpretationown data

    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.

    “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.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    Participants made no report of gastrointestinal distress or alterations of GI transit time throughout the course of the initial study.

    “Participants made no report of gastrointestinal (GI) distress or alterations of GI transit time throughout the course of the initial study.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Approval for this study was granted by the Cork Clinical Research Ethics Committee.

    “Approval for this study was granted by the Cork Clinical Research Ethics Committee.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    3-hydroxy-isovaleric acid has been demonstrated to have efficacy for inhibiting muscle wasting when used in conjunction with physical exercise.

    “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]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [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

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    All reported p values were corrected for multiple comparisons using the Benjamini-Hochberg false discovery rate method.

    “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.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [47] source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    PAG has been associated with a lean phenotype.

    “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]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [42] source

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The compound 3-hydroxy-isovaleric acid is 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 high-intensity exercise.

    “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]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
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27 of 27
  • 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”
1 of 1

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Each contradiction between two passages listed here was confirmed by an independent check.

  • Glutamine is reported as both lower and higher in athletes

    Minor

    The results say urinary glutamine was lower in athletes than in controls, but the discussion lists glutamine among metabolites raised in athletes.

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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
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
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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