Effect of Exercise, Physical Activity, and Performance on Human Gut Microbes and Microbial Metabolome

A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Microbiology and Ecological Metabolomics".

Deadline for manuscript submissions: closed (15 February 2022) | Viewed by 24238

Special Issue Editor


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Guest Editor
Faculty of Sport and Health Sciences, University of Jyvaskyla, 40014 Jyvaskyla, Finland
Interests: gut microbiota; exercise; health and metabolism

Special Issue Information

Dear Colleagues,

Humans carry ~100 trillion tiny microbial cells inhabiting the gastrointestinal tract, with whom they have been living for a long time in a symbiotic mutualistic relationship. Accumulating data shows that the gut microbiota importantly affects host metabolic phenotypes through the production of metabolites from the diet ingested. Recent studies have shown that exercise and physical performance have an impact on the gut microbiome. However, controversies exist and thus more research in the field is needed. Especially, the role of microbial metabolites in transmitting the effects of exercise from the gut to the whole body should be emphasized. We, therefore, invite contributions to this Special Issue on the effect of exercise, physical activity, and performance on human gut microbiota composition and, most importantly, on the fecal metabolome. Interventional studies are particularly encouraged but all cross-sectional studies are also warmly welcome. Studies on gut microbiota in physically inactive individuals with symptoms of metabolic syndrome are also of interest.

Dr. Satu Pekkala
Guest Editor

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Keywords

  • Gut microbiota
  • Microbial metabolites
  • Exercise
  • Physical performance
  • Physical inactivity
  • Metabolism
  • Metabolic syndrome
  • Obesity

Published Papers (6 papers)

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Research

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18 pages, 2022 KiB  
Article
Exercise and Interorgan Communication: Short-Term Exercise Training Blunts Differences in Consecutive Daily Urine 1H-NMR Metabolomic Signatures between Physically Active and Inactive Individuals
by Leon Deutsch, Alexandros Sotiridis, Boštjan Murovec, Janez Plavec, Igor Mekjavic, Tadej Debevec and Blaž Stres
Metabolites 2022, 12(6), 473; https://doi.org/10.3390/metabo12060473 - 24 May 2022
Cited by 4 | Viewed by 2090
Abstract
Physical inactivity is a worldwide health problem, an important risk for global mortality and is associated with chronic noncommunicable diseases. The aim of this study was to explore the differences in systemic urine 1H-NMR metabolomes between physically active and inactive healthy young [...] Read more.
Physical inactivity is a worldwide health problem, an important risk for global mortality and is associated with chronic noncommunicable diseases. The aim of this study was to explore the differences in systemic urine 1H-NMR metabolomes between physically active and inactive healthy young males enrolled in the X-Adapt project in response to controlled exercise (before and after the 3-day exercise testing and 10-day training protocol) in normoxic (21% O2), normobaric (~1000 hPa) and normal-temperature (23 °C) conditions at 1 h of 50% maximal pedaling power output (Wpeak) per day. Interrogation of the exercise database established from past X-Adapt results showed that significant multivariate differences existed in physiological traits between trained and untrained groups before and after training sessions and were mirrored in significant differences in urine pH, salinity, total dissolved solids and conductivity. Cholate, tartrate, cadaverine, lysine and N6-acetyllisine were the most important metabolites distinguishing trained and untrained groups. The relatively little effort of 1 h 50% Wpeak per day invested by the untrained effectively modified their resting urine metabolome into one indistinguishable from the trained group, which hence provides a good basis for the planning of future recommendations for health maintenance in adults, irrespective of the starting fitness value. Finally, the 3-day sessions of morning urine samples represent a good candidate biological matrix for future delineations of active and inactive lifestyles detecting differences unobservable by single-day sampling due to day-to-day variability. Full article
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15 pages, 4431 KiB  
Article
Gut Microbiota and Serum Metabolome in Elite Cross-Country Skiers: A Controlled Study
by Jukka E. Hintikka, Eveliina Munukka, Maarit Valtonen, Raakel Luoto, Johanna K. Ihalainen, Teemu Kallonen, Matti Waris, Olli J. Heinonen, Olli Ruuskanen and Satu Pekkala
Metabolites 2022, 12(4), 335; https://doi.org/10.3390/metabo12040335 - 07 Apr 2022
Cited by 9 | Viewed by 4047
Abstract
Exercise has been shown to affect gut the microbiome and metabolic health, with athletes typically displaying a higher microbial diversity. However, research on the gut microbiota and systemic metabolism in elite athletes remains scarce. In this study, we compared the gut microbiota profiles [...] Read more.
Exercise has been shown to affect gut the microbiome and metabolic health, with athletes typically displaying a higher microbial diversity. However, research on the gut microbiota and systemic metabolism in elite athletes remains scarce. In this study, we compared the gut microbiota profiles and serum metabolome of national team cross-country skiers at the end of an exhausting training and competitive season to those of normally physically-active controls. The gut microbiota were analyzed using 16S rRNA amplicon sequencing. Serum metabolites were analyzed using nuclear magnetic resonance. Phylogenetic diversity and the abundance of several mucin-degrading gut microbial taxa, including Akkermansia, were lower in the athletes. The athletes had a healthier serum lipid profile than the controls, which was only partly explained by body mass index. Butyricicoccus associated positively with HDL cholesterol, HDL2 cholesterol and HDL particle size. The Ruminococcus torques group was less abundant in the athlete group and positively associated with total cholesterol and VLDL and LDL particles. We found the healthier lipid profile of elite athletes to co-occur with known health-beneficial gut microbes. Further studies should elucidate these links and whether athletes are prone to mucin depletion related microbial changes during the competitive season. Full article
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10 pages, 1080 KiB  
Article
Non-Invasive Monitoring of Inflammation in Inflammatory Bowel Disease Patients during Prolonged Exercise via Exhaled Breath Volatile Organic Compounds
by Ben Henderson, Joris Meurs, Carlijn R. Lamers, Guilherme Lopes Batista, Dušan Materić, Carlo G. Bertinetto, Coen C. W. G. Bongers, Rupert Holzinger, Frans J. M. Harren, Jeroen J. Jansen, Maria T. E. Hopman and Simona M. Cristescu
Metabolites 2022, 12(3), 224; https://doi.org/10.3390/metabo12030224 - 03 Mar 2022
Cited by 8 | Viewed by 3071
Abstract
The aim of this study was to investigate volatile organic compounds (VOCs) in exhaled breath as possible non-invasive markers to monitor the inflammatory response in inflammatory bowel disease (IBD) patients as a result of repeated and prolonged moderate-intensity exercise. We included 18 IBD [...] Read more.
The aim of this study was to investigate volatile organic compounds (VOCs) in exhaled breath as possible non-invasive markers to monitor the inflammatory response in inflammatory bowel disease (IBD) patients as a result of repeated and prolonged moderate-intensity exercise. We included 18 IBD patients and 19 non-IBD individuals who each completed a 30, 40, or 50 km walking exercise over three consecutive days. Breath and blood samples were taken before the start of the exercise event and every day post-exercise to assess changes in the VOC profiles and cytokine concentrations. Proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) was used to measure exhaled breath VOCs. Multivariate analysis, particularly ANOVA-simultaneous component analysis (ASCA), was employed to extract relevant ions related to exercise and IBD. Prolonged exercise induces a similar response in breath butanoic acid and plasma cytokines for participants with or without IBD. Butanoic acid showed a significant correlation with the cytokine IL-6, indicating that butanoic acid could be a potential non-invasive marker for exercise-induced inflammation. The findings are relevant in monitoring personalized IBD management. Full article
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22 pages, 2970 KiB  
Article
Physical Activity and Dietary Composition Relate to Differences in Gut Microbial Patterns in a Multi-Ethnic Cohort—The HELIUS Study
by Veera Houttu, Ulrika Boulund, Mary Nicolaou, Adriaan Georgius Holleboom, Aldo Grefhorst, Henrike Galenkamp, Bert-Jan van den Born, Koos Zwinderman and Max Nieuwdorp
Metabolites 2021, 11(12), 858; https://doi.org/10.3390/metabo11120858 - 09 Dec 2021
Cited by 4 | Viewed by 3641
Abstract
Physical activity (PA) at recommended levels contributes to the prevention of non-communicable diseases, such as atherosclerotic cardiovascular disease (asCVD) and type 2 diabetes mellitus (T2DM). Since the composition of the gut microbiota is strongly intertwined with dietary intake, the specific effect of exercise [...] Read more.
Physical activity (PA) at recommended levels contributes to the prevention of non-communicable diseases, such as atherosclerotic cardiovascular disease (asCVD) and type 2 diabetes mellitus (T2DM). Since the composition of the gut microbiota is strongly intertwined with dietary intake, the specific effect of exercise on the gut microbiota is not known. Moreover, multiple other factors, such as ethnicity, influence the composition of the gut microbiota, and this may be derived by distinct diet as well as PA patterns. Here we aim to untangle the associations between PA and the gut microbiota in a sample (n = 1334) from the Healthy Life In an Urban Setting (HELIUS) multi-ethnic cohort. The associations of different food groups and gut microbiota were also analyzed. PA was monitored using subjective (n = 1309) and objective (n = 162) methods, and dietary intake was assessed with ethnic-specific food frequency questionnaire (FFQ). The gut microbiota was profiled using 16S rRNA gene amplicon sequencing, and the functional composition was generated with the Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt2). Associations were assessed using multivariable and machine learning models. In this cohort, a distinct gut microbiota composition was associated with meeting the Dutch PA norm as well as with dietary intake, e.g., grains. PA related parameters such as muscle strength and calf circumference correlated with gut microbiota diversity. Furthermore, gut microbial functionality differed between active and sedentary groups. Differential representation of ethnicities in active and sedentary groups in both monitor methods hampered the detection of ethnic-specific effects. In conclusion, both PA and dietary intake were associated with gut microbiota composition in our multi-ethnic cohort. Future studies should further elucidate the role of ethnicity and diet in this association. Full article
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14 pages, 1934 KiB  
Article
The Effect of Kefir Supplementation on Improving Human Endurance Exercise Performance and Antifatigue
by Mon-Chien Lee, Wei-Lun Jhang, Chia-Chia Lee, Nai-Wen Kan, Yi-Ju Hsu, Chin-Shan Ho, Chun-Hao Chang, Yi-Chen Cheng, Jin-Seng Lin and Chi-Chang Huang
Metabolites 2021, 11(3), 136; https://doi.org/10.3390/metabo11030136 - 25 Feb 2021
Cited by 11 | Viewed by 5556
Abstract
Kefir is an acidic, carbonated, and fermented dairy product produced by fermenting milk with kefir grains. The Lactobacillus species constitutes an important part of kefir grains. In a previous animal study, kefir effectively improved exercise performance and had anti-fatigue effects. The purpose of [...] Read more.
Kefir is an acidic, carbonated, and fermented dairy product produced by fermenting milk with kefir grains. The Lactobacillus species constitutes an important part of kefir grains. In a previous animal study, kefir effectively improved exercise performance and had anti-fatigue effects. The purpose of this research was to explore the benefits of applying kefir to improve exercise performance, reduce fatigue, and improve physiological adaptability in humans. The test used a double-blind crossover design and supplementation for 28 days. Sixteen 20–30 year-old subjects were divided into two groups in a balanced order according to each individual’s initial maximal oxygen uptake and were assigned to receive a placebo (equal flavor, equal calories, 20 g/day) or SYNKEFIR™ (20 g/day) every morning. After the intervention, there were 28 days of wash-out, during which time the subjects did not receive further interventions. After supplementation with SYNKEFIR™, the exercise time to exhaustion was significantly greater than that before ingestion (p = 0.0001) and higher than that in the Placebo group by 1.29-fold (p = 0.0004). In addition, compared with the Placebo group, the SYNKEFIR™ administration group had significantly lower lactate levels in the exercise and recovery (p < 0.05). However, no significant difference was observed in the changes in the gut microbiota. Although no significant changes in body composition were found, SYNKEFIR™ did not cause adverse reactions or harm to the participants’ bodies. In summary, 28 days of supplementation with SYNKEFIR™ significantly improved exercise performance, reduced the production of lactic acid after exercise, and accelerated recovery while also not causing any adverse reactions. Full article
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Review

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22 pages, 1042 KiB  
Review
Gut Microbiota, Microbial Metabolites and Human Physical Performance
by Sanna Lensu and Satu Pekkala
Metabolites 2021, 11(11), 716; https://doi.org/10.3390/metabo11110716 - 21 Oct 2021
Cited by 12 | Viewed by 4683
Abstract
Trillions of microbes inhabiting the gut modulate the metabolism of the host. Cross-sectional studies have reported associations between physical performance and the gut microbiota (GM). Physical activity seems to increase GM diversity and the abundance of certain health-beneficial microbes. We reviewed the evidence [...] Read more.
Trillions of microbes inhabiting the gut modulate the metabolism of the host. Cross-sectional studies have reported associations between physical performance and the gut microbiota (GM). Physical activity seems to increase GM diversity and the abundance of certain health-beneficial microbes. We reviewed the evidence from longitudinal studies on the connection between physically active lifestyle or long-term exercise interventions and the GM. We made literature searches using databases of Web of Science and PubMed Medline to collect human studies showing or not the associations between the GM and exercise. Many controversies exist in the studies. However, the longitudinal studies show that frequently, medium-intensity endurance exercise has yielded most beneficial effects on the GM, but the results vary depending on the study population and exercise protocol. In addition, the literature shows that certain microbes own the potency to increase physical activity and performance. Generally, a physically active lifestyle and exercise associate with a “healthy” GM. However, in previously sedentary subjects, the exercise-induced improvements in the GM seem to disappear unless the active lifestyle is continued. Unfortunately, several studies are not controlled for the diet. Thus, in the future, more longitudinal studies on the GM and physical performance are needed, with detailed dietary information. Full article
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