Strenuous Physical Training, Physical Fitness, Body Composition and Bacteroides to Prevotella Ratio in the Gut of Elderly Athletes

Abstract

Regular physical activity seems to have a positive effect on the microbiota composition of the elderly, but little is known about the added possible benefits of strenuous endurance training. To gain insight into the physiology of the elderly and to identify biomarkers associated with endurance training, we combined different omics approaches. We aimed to investigate the gut microbiome, plasma composition, body composition, cardiorespiratory fitness, and muscle strength of lifetime elderly endurance athletes (LA) age 63.5 (95% CI 61.4, 65.7), height 177.2 (95% CI 174.4, 180.1) cm, weight 77.8 (95% CI 75.1, 80.5) kg, VO2max 42.4 (95% CI 39.8, 45.0) ml.kg–1.min–1 (n = 13) and healthy controls age 64.9 (95% CI 62.1, 67.7), height 174.9 (95% CI 171.2, 178.6) cm, weight 83.4 (95% CI 77.1, 89.7) kg, VO2max 28.9 (95% CI 23.9, 33.9), ml.kg–1.min–1 (n = 9). Microbiome analysis was performed on collected stool samples further subjected to 16S rRNA gene analysis. NMR-spectroscopic analysis was applied to determine and compare selected blood plasma metabolites mostly linked to energy metabolism. The machine learning (ML) analysis discriminated subjects from the LA and CTRL groups using the joint predictors Bacteroides 1.8E + 00 (95% CI 1.1, 2.5)%, 3.8E + 00 (95% CI 2.7, 4.8)% (p = 0.002); Prevotella 1.3 (95% CI 0.28, 2.4)%, 0.1 (95% CI 0.07, 0.3)% (p = 0.02); Intestinimonas 1.3E-02 (95% CI 9.3E-03, 1.7E-02)%, 5.9E-03 (95% CI 3.9E-03, 7.9E-03)% (p = 0.002), Subdoligranulum 7.9E-02 (95% CI 2.5E-02, 1.3E-02)%, 3.2E-02 (95% CI 1.8E-02, 4.6E-02)% (p = 0.02); and the ratio of Bacteroides to Prevotella 133 (95% CI -86.2, 352), 732 (95% CI 385, 1079.3) (p = 0.03), leading to an ROC curve with AUC of 0.94. Further, random forest ML analysis identified VO2max, BMI, and the Bacteroides to Prevotella ratio as appropriate, joint predictors for discriminating between subjects from the LA and CTRL groups. Although lifelong endurance training does not bring any significant benefit regarding overall gut microbiota diversity, strenuous athletic training is associated with higher cardiorespiratory fitness, lower body fat, and some favorable gut microbiota composition, all factors associated with slowing the rate of biological aging.

Gut Microbiota, Microbial Metabolites and Human Physical Performance

“…Because Akkermansia muciniphila is the only known species of this phylum, the difference was further quantified with PCR, which confirmed that A. muciniphila was more abundant in the physically active than inactive women [30]. In another cross-sectional study, Verrucomicrobia was also shown to be more abundant in elderly men with lifelong training background compared with controls [31]. It is not known how a physically active lifestyle would increase the abundance of Akkermansia, but it could be that the dietary habits of the active individuals play a role.…”

“…The sole known species of the Faecalibacterium genus, Faecalibacterium prausnitzii is one of the most abundant commensals with important antiinflammatory functions [61][62][63], and we have shown that this health-beneficial bacterium can ameliorate non-alcoholic fatty liver disease, too [64]. The abundance of F. prausnitzii has been shown to be higher in elite endurance runner women [38] and in healthy, physically active, premenopausal women than in sedentary counterparts [30], although the situation was contrary among active elderly men [31]. However, it seems that exercise may increase the abundance of Faecalibacterium and whether the increased abundance of this anti-inflammatory bacterium could be related to some of the anti-inflammatory effects of exercise (e.g., [65]), should be studied in the future.…”

“…The lifelong exercise was detectable as distinct differences in the selected GM genera, beta-diversity, Bacteroides to Prevotella ratio and in the physiological fitness markers. However, among the best predictors for discriminating the active ones from the controls was the Bacteroides to Prevotella ratio, in addition to maximal oxygen intake (VO 2 max) and BMI [31]. Similarly, in studies of elite top-level endurance type of athletes (males and females, aged in Poland [37] and in Japan (females, ~20 years old) [38], distinct differences in the GM have been depicted, in comparison to the respective control population.…”

“…There are also cross-sectional studies on the effects of lifelong exercise on the GM and markers of physical fitness. Recently, Šoltys et al [31] compared the groups of training athletes and controls, who were healthy elderly men (60-70 years) in Slovakia. Šoltys and co-workers were able to show that lifelong strenuous endurance training affects the GM composition in comparison to the controls [31].…”

“…Recently, Šoltys et al [31] compared the groups of training athletes and controls, who were healthy elderly men (60-70 years) in Slovakia. Šoltys and co-workers were able to show that lifelong strenuous endurance training affects the GM composition in comparison to the controls [31]. The training background did not affect the alpha-diversity of the GM, calculated as the Shannon, Simpson or Chao1 indices, but at the genus level, the trained men had higher relative abundance of e.g., Phascolarctobacterium, Prevotella, and Subdoligranulum than the controls, and lower abundance of Bacteroides, Blautia, Faecaelibacterium and Roseburia.…”