Gut Microbiota, Microbial Metabolites and Human Physical Performance
Abstract
:1. Introduction
2. Cross-Sectional Studies Have Reported Associations between Exercise, Physical Performance, and the Gut Microbiota in Humans—Some Examples
3. Longitudinal Studies Showing Effects of Longer-Term Exercise on the Human Gut Microbiota and Microbial Metabolism
3.1. Endurance Exercise and Gut Microbiota
3.2. The Effects of Combined Resistance and Aerobic Exercise on the Gut Microbiota
3.3. High Intensity Exercise or Strenuous Training and Gut Microbiota
4. The Effects of Shorter-Term Exercise Challenges on the Gut Microbiome
5. Certain Gut Microbes Can Increase Physical Performance
6. Conclusions
Supplementary Materials
Funding
Conflicts of Interest
References
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Training Mode | Specification and Duration of Training | Study Population | n of Subjects | Outcome | Reference in the List of References |
---|---|---|---|---|---|
ENDURANCE TRAINING | |||||
Aerobic endurance training, increasing in duration (min) and from 60 to 75% of VO2max | 3x per wk, 40–60 min for 6 wks, either ergometer cycling or treadmill running; post-training washout period for 6 wks | lean and obese, physically inactive women and men | n = 14 obese (of which n = 11 female), n = 18 lean (of which n = 9 female) | All subjects VO2max ↑, Fat % ↓ In lean Bacteroides ↓ Faecalibacterium ↑, In obese Bacteroides ↑, Faecalibacterium ↓; SCFA ↑ in feces of lean following exercise. Effects of exercise were mostly reversed during the washout. Diet was followed up and subjects were asked to maintain it; Results of diet follow-up not reported | Allen et al., 2018, [42] |
Aerobic endurance training | ergometer cycling 3x per wk, for 6 wks, additional control period included for study subjects | overweighed and physically inactive women | n = 17 (served as own controls) | VO2max ↑, Android fat ↓, Proteobacteria ↓, Akkermansia ↑ Food records were collected throughout, diet remained mainly unaffected during exercise intervention | Munukka et al., 2018, [43] |
Aerobic endurance training; cross-over | ergometer cycling 3x per wk, starting 30 min at 60% of VO2max level, gradually increasing in duration and intensity, for 5 wks | >60 yrs old, healthy Japanese men | n = 31 having both training and control periods | Clostridium difficile ↓, Oscillospira ↑ and VO2max ↑ and HDL ↑, hepatic fat ↓ during exercise Of the metagenomic functions of GM, genetic information processing and metabolism of nucleotides ↑ Diet followed up with questionnaires and food records, changes in diet but they were similar during control and exercise periods | Taniguchi et al., 2018, [44] |
Aerobic endurance-type, at different intensity levels | 5x per wk, for 6 months; BIKE = commuting by bike, MOD, moderate exercise (50% of VO2 peak); VIG, vigorous exercise (70% of VO2peak); CON, continued habitual sedentary living | overweight or obese, inactive 20–45 yrs old women and men | BIKE, n = 19; MOD, n = 31; VIG, n = 24; CON, n = 14 | Physical performance ↑ and Fat % ↓ in all exercise groups, Exercise ineffective on individual GM abundances VIG: GM α-diversity (Shannon index) ↑ after 3 months MOD: Functional capacity of GM ↑ after 3 moths Food diaries were collected, and changes occurred in exercising groups (intake of fat) | Kern et al., 2020, [45] |
Endurance training (decreasing training load) | 2 wk swimming 32.4 ± 4.8 km/wk, then 2 wk 19.6 ± 8.2 km/wk, then 2 wk 11.3 ± 8.1 km/wk | 18–24 yrs old, collegiate swimmers | n = 13 | GM α-diversity ↓ as well as abundance of Coprococcus and Faecalibacterium ↓ along the training volume, no changes in changes in weight, fat mass or fat-free mass | Hampton-Marcell et al., 2020 [46] |
Moderate-intensity aerobic training | 4x per wk, running (at level 50–70% of max. heart rate) 30 min for 12 wks | 12–14 yrs old, healthy or having subthreshold mood symptoms | n = 49 mood syndrome and n = 142 healthy of which n = 96 were training | Exercise was ineffective No information about the diet | Wang et al., 2021, [47] |
COMBINED TRAINING or STUDIES WITH VARIOUS TRAINING MODES | |||||
Endurance/Strength/Elite athletes | Endurance: running 4x per wk >30 min (of which 1 supervised); Strength: at gym 4x per wk (of which 2 supervised). Training loads were ↑, total duration 6 wks | Inactive 20–45 yrs old, BMI 20–35 kg/m2, healthy women and men + elite athletes | n = 42 men and women → n = 13 endurance, n = 12 strength, n = 11 ctrl and additional group of elite athletes (n = 13) | Different types of exercise induced some moderate health-related effects, but no systematic effects on GM Diet changed in strength group, but other groups remained unchanged. Diet was accounted in PCA-models. | Moitinho-Silva et al., 2021, [48] |
Combined resistance and aerobic training, increasing load (with or without whey supplement) | 3x per wk, for 8 wks, each session included moderate aerobic training (18–32 min) + progressive, machine-based repetitive resistance exercises (starting ~70% of one-repetition max. level) | overweight and physically inactive women and men, ~35 yrs old | n = 25 (having exercise training only, we did not include whey groups) | VO2max ↑, Fat % ↓, Lean mass ↑, No significant effect on the GM α-diversity or metabolic pathways In exercise group diet remained unchanged | Cronin et al., 2018, [49] |
Combined resistance and aerobic training, increasing load | 3x per wk for 8 wks; session included moderate aerobic training (18–32 min) + progressive, machine-based repetitive resistance exercises (starting ~70% of one-repetition max. level) | overweight, ~25 yrs old inactive males and females diagnosed with inflammatory bowel disease (IBD) | n = 13 exercise group, n = 7 control group | In exercise group: Fat % ↓, Lean mass ↑, α-diversity of Archaea species ↑, no effects on IBD activity scores, mood or inflammation No significant effect on GM α-diversity or metabolic pathways No information about diet | Cronin et al., 2019, [50] |
Combined strength/endurance/stretching training | 3x per wk, 90 min per session for 6 months | type 2 diabetic males | n = 30 | VO2max ↑, weight and fat-% ↓, glycemia ↑ Intestinal mycetes overgrowth ↓, zonulin (intestinal leakage) ↓, systemic inflammation ↓ No information about diet | Pasini et al., 2019, [51] |
Combined strength and endurance training | 3–5x per wk, for 8 wks, 10 free-weight or rubber band strength exercises and individualized endurance training (first walking/jogging then interval training) | non-alcoholic fatty liver disease patients, who completed >70% of training, age 18–70, BMI 18.5–45 kg/m2 | n = 41 | VO2max ↑, Fat % and weight ↓, hepatic illness scores ↑, inflammation ↓ Metagenomic richness ↑, Bacteroidetes and Euryarchaeota ↑, Actinobacteria ↓ Diet was not controlled/followed up | Huber et al., 2019, [52] |
Trunk muscle strength or aerobic training | 1 h per day for 12 wks; Aerobic = brisk walking (≥3 METs); strength = trunk muscle training (free-weight gymnastics) | healthy >60 yrs old women | n = 14 strength, n = 17 aerobic training | Both training modes: physical performance ↑, strength and elasticity ↑ Aerobic training: Bacteroides ↑, Clostridium subcluster XIVa ↓ Strength training: Clostridium cluster IX ↑ Diet was followed up with questionnaires and no differences during the study between groups | Morita et al., 2019, [53] |
Combined aerobic and resistance training | 4x per wk, ~60 min per session for 8 wks, gymnastics (= aerobic) and rubber band (= resistance) training with increase in training load | previously inactive women, ≥60 yrs old | n = 6 sedentary controls, n = 6 training | Firmicutes, Phascolarctobacterium, Mitsuokella ↑ after training, no effect on alpha diversity of GM, exercise improved physical performance No information about diet | Zhong et al., 2021 [54] |
Combined strength and aerobic exercise | 2x per wk, for 12 wks, bicycle ergometer, strength exercises | pediatric obese patients and non-obese, age 7–12 | n = 39 obese → n = 25 exercise, n = 14 control, n = 14 non-obese | Plasma glucose ↓, Dynamic strength ↑ Proteobacteria and Gammaproteobacteria ↓ Fecal branched chain amino acids, formate, alanine and glucose ↓ | Quiroga et al., 2020, [55] |
HIGH-INTENSITY TRAINING | |||||
Increasing sprint interval training or moderate-intensity aerobic training (both used cycling) | Intervals: 4–6x 30 work, 4 min rest; 3x per wk for 2 wks Endurance: 3x per wk for 2 wks, 40–60 min | obese and sedentary men and women who were diabetic or prediabetic, age 40–55 yrs | n = 16 (n = 9 type 2 diabetic, n = 17 prediabetic) | Interval: VO2max ↑, Fat %↓, Both training modes: Firmicutes/Bacteroidetes ↓, Clostridium ↓, Blautia ↓ Moderate intensity: Faecalibacterium ↑ No information about diet, it was asked to maintain unchanged | Motiani et al., 2020, [56] |
High intensity interval ergometer training, short-term | 3x per wk for 3 wks using ergometer; 8–12 bouts repeated at VO2max level, 1 bout = 60 s work + 75 s rest | lean and obese men, sedentary or less than 3 hrs endurance activity weekly | n = 14 lean, n = 15 obese | Insulin sensitivity and cardiovascular fitness ↑, no changes in GM, some microbes associated with insulin sensitivity among obese Diet differed between the groups before, but was not followed-up during intervention | Rettedal et al., 2020, [57] |
High intensity interval training: combined strength and endurance with increasing load | 3x per wk for 12 wks, supervised 70 min. sessions containing high-intensity running/biking sessions ~80–95% of VO2max or HRmax level, high-intensity resistance and calisthenics exercises (e.g., kettle ball, squats), warm-up, cooldown and stretching | non-smoking, overweight/obese men, prediabetic | n = 39 → n = 19 sedentary controls, n = 14 exercise responsive and n = 6 non-responsive, validation study with n = 30 obese men | Following HIIT, insulin sensitivity ↑ in responders but not in non-responders, GM α- or β-diversity unaffected, abundances of species among Firmicutes, Bacteroidetes, Proteobacteria changed in response to exercise, e.g., Alistipes putredinis ↓, Bactroides xylanisolvens ↓, Lachnospiraceae bacterium ↑ in responders By machine-learning algorithms GM signatures were shown to predict exercise responses in a validation study Diet was monitored with questionnaires and groups did not differ | Liu et al., 2020, [58] |
STRENOUS TRAINING | |||||
Strenous, high-intensity exercise | 4 days, 51-km cross-country ski march | healthy soldiers | n = 73 | Gut permeability ↑, GM diversity ↑ Verrucomicrobia, Tenericutes, Spirochaetes, Lentisphera, Fusobacteria and Firmicutes ↑ Euarchaeota ↓ Fecal metabolism of phenylalanine, tryptophan and tyrosine ↓ Fecal metabolism of carbohydrates, fatty acids and secondary bile acids ↓ | Karl et al., 2017 [59] |
Continuous rowing | 33 days, 5000 km transatlantic rowing, each athletic rowed 395 hrs | healthy, elite male athletes (~26 yrs) | n = 4 | VO2max unchanged, GM α-diversity ↑, butyrate producing GM (Roseburia hominis, Subdoligranulum) ↑, Bacteroides finegoldii ↓; in functional metabolic pathways of GM gene products, synthesis of L-isoleucine, L-lycine ↑, S-adenosyl-L-methionine ↑, long chain fatty acids ↑, fatty acid elongation and glycolysis ↑ Diet was followed up, and macronutrient intake remained constant, but diet changed during rowing | Keohane et al., 2019, [60] |
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Lensu, S.; Pekkala, S. Gut Microbiota, Microbial Metabolites and Human Physical Performance. Metabolites 2021, 11, 716. https://doi.org/10.3390/metabo11110716
Lensu S, Pekkala S. Gut Microbiota, Microbial Metabolites and Human Physical Performance. Metabolites. 2021; 11(11):716. https://doi.org/10.3390/metabo11110716
Chicago/Turabian StyleLensu, Sanna, and Satu Pekkala. 2021. "Gut Microbiota, Microbial Metabolites and Human Physical Performance" Metabolites 11, no. 11: 716. https://doi.org/10.3390/metabo11110716