Open access peer-reviewed chapter
Abstract
The gut microbiota is believed to have a major impact on human health and disease. It is involved in barrier functions and maintenance of homeostasis. It provides nutrients and metabolites, participates in a signaling network, regulates epithelial development, and influences the immune system as well as protects the intestinal mucosa from the aggression of pathogenic microorganisms. There is growing evidence that physical activity has an impact on the gut microbiota. Recent studies in animals and humans suggest that regular physical activity increases the presence of beneficial microbial species and improves host health. However, some specific differences should be noted: different forms of physical activity, frequency or intensity, aerobic or resistance training, and benefits and consequences for amateur or competitive athletes. Because the positive role of physical activity can have an impact on health and various types of diseases, the results of research studies in this area are increasingly becoming the focus of scientific interest. In addition, probiotic supplements modulate intestinal microbial flora, and the ability of probiotics to modulate perturbations in immune function after exercise highlights their potential for use in individuals exposed to high levels of physical activity.
Keywords
- gut microbiota
- immune system
- physical exercise
- health
- probiotics
1. Introduction
The human gastrointestinal tract is inhabited by hundreds of thousands of microorganisms that represent highly diverse microbiota. Gut microbiota comprises a metabolically active and complex ecosystem (bacteria, archaea, viruses, and unicellular eukaryotes) that colonizes the digestive tract soon after birth [1]. It has a crucial role in establishing a dynamic association with the human organism, having crucial roles in several physiological and pathological processes [2, 3]. It protects the host from the colonization of pathogens and is linked to nutrient digestion and absorption as well as to immunological, metabolic, and motor functions [4].
In the adult gut microbiota, four major microbial phyla are known to represent over 90% of the bacterial components:
The development and maturation of gut microbiota is a dynamic process that starts in early life. Its composition may be affected by several intrinsic and extrinsic factors, like mode of delivery, mother’s age, diet and metabolic status, type of feeding, family genetics, lifestyle, exercise, immunological factors, drugs like antibiotics, and availability of nutrients [7, 8, 9, 10, 11, 12, 13]. Colonization of the infant’s gut was thought to begin at birth, but scientific evidence has provided indications of bacterial presence in the placenta, umbilical cord, and amniotic fluid in healthy full-term pregnancies [14, 15, 16]. These findings suggest that microbial exposure may start before delivery, allowing colonization of the fetus with maternal microbiota. Another driver affecting the microbial colonization of the infant’s intestine represents the delivery mode [17]. Vagina-associated microbes such as
2. Microbiota metabolites in health and disease
Exercise or physical activity can greatly affect the composition of the gut microbiota. It improves several metabolic and inflammatory parameters in chronic diseases and has been used as a therapeutic strategy in chronic diseases. In this chapter, we summarize several experimental findings on the possible mechanisms by which physical activity could influence gut microbiota. We also discuss the health benefits of physical activity, probiotic consumption, and microbiota diversity. The modification in the composition and function of the gut microbiota has an impact on intestinal permeability, digestion, metabolism, and immune responses. Many diseases, from digestive to metabolic problems as well as immunological and neuropsychiatric disorders, are linked to the pro-inflammatory state caused by the alternation of gut microbiota balance [13]. The gut microbiome contributes to digestion and promotes food absorption for host energy production. Its fermentation of non-digestible dietary residues leads to metabolites such as short-chain fatty acids (SCFAs, like butyrate, acetate, and propionate), which modulate the host energy balance increasing the availability of nutrients [25]. Fermented SCFAs, secreted into the gut lumen, exceed the epithelial barrier and are released into the bloodstream. They can be used as energy sources by the intestinal microbiota and by the host cells. They could provide nearly 10% of our daily energy requirements [26]. Butyrate is used as an energy source primarily by epithelial cells in the colon. Propionate is involved in liver gluconeogenesis [27]. It also decreases serum cholesterol levels, inhibits fatty-acid synthesis, and may be involved in weight control by stimulating satiety [28]. Acetate is metabolized in muscle tissue and can also cross the blood-brain barrier. It is used as a substrate for liver cholesterol and fatty acid synthesis [29, 30], increases colonic blood flow and oxygen uptake, and enhances ileal motility by affecting ileal contractions [31].
SCFAs can also contribute to shaping the gut environment and colon physiology, participating in different host-signaling mechanisms as well as possessing some anti-inflammatory effects [32, 33, 34]. Butyrate regulates the neutrophil function and migration, increases the expression of tight junction proteins in colon epithelia, enhances gut integrity, and activates intraepithelial lymphocytes (IELs), which express cytokines (IFN-γ and keratinocyte growth factor) to protect epithelial cells from injury [35, 36].
Besides producing SCFAs, bacterial species of the gut microbiota synthesize glycan, amino acids, and vitamins (K, B12, biotin, folate, and thiamine) and participate in the digestion of polysaccharides, increasing the amount of glucose in the liver and, therefore, increasing lipogenesis [33, 37, 38, 39].
Protective functions of microbiota are performed also through competition with pathogens for nutrients and receptors and the production of antimicrobial molecules and metabolites to avoid colonization by pathogens [40]. Through ligands from commensal bacteria (lipopolysaccharide, LPS), the gut microbiota influences the mucosal immune system development and function [41].
Gastrointestinal mucosa is a complex system acting as a physical barrier that regulates epithelial permeability. The regulation of trans-epithelial permeability allows the absorption of nutrients from the intestinal lumen through the cells lining the gut wall into the blood circulation [42]. Gut bacteria-epithelial cell interactions have been suggested as key contributors to epithelial permeability. Dysregulation of the gut microbiota and disruption of the gut mucosa enable harmful substances to pass through the barrier and can lead to the development of several chronic diseases [13, 43]. Gut dysbiosis, characterized by an imbalance in the composition and activity of gut microbial communities, has been linked to functional and inflammatory disorders [44, 45].
3. Gut microbiota composition and physical activity
Physical activity, especially moderate, has a positive effect on our body [34]. It can reduce metabolic and inflammatory diseases and influence the microbiota and health of humans and animals. Physical activity can be divided into the moderate level (< 70% VO2 max) and high-intensity level (> 70% VO2max). According to published studies, moderate physical activity has a positive effect on intestinal permeability, absorption and assimilation of food, and excretion of toxic metabolites [46]. In contrast, higher exercise intensity can negatively affect the digestive system and lead to the exercise-induced gastrointestinal syndrome, which affects 70% of athletes [47]. This may be the result of exercise-induced changes in the immune system of the digestive tract, leading to an increase in the inflammatory response and gastrointestinal symptoms [48].
The balance between exercise intensity, performance, and microbiota composition should be monitored for a long-time to optimize performance, health, and well-being and limit gastrointestinal syndromes.
3.1 Associations between physical activity and changes in gut microbiota in animal studies
Many animal experiments have been performed on mice and rodents, which are good models for mimicking human physiology. In animals, different forms of exercise, especially voluntary and forced, resulted in different effects on the composition of the microbiome. Many germ-free animal studies have indicated the relationship between gut microbiota and host function [49, 50]. Alteration in gut microbiota and its metabolites can affect the structure of the mucus layer and immune system after gut microbiota colonization in germ-free animals. It was demonstrated [50] that exercise training triggered changes in gut microbiota community structure in donor mice and in gut physiology in recipient mice after 5 weeks of gut microbiota transplantation and colonization. Thus, the composition of the gut microbiota of recipient mice is dependent on the physical activity of their respective donors. This suggests that physical training directly alters the host response through cytokines and the production of intestinal metabolites.
SCFAs upregulated after exercise contribute to improved energy production and reduce inflammation in the gut of physically active individuals [51]. In addition, voluntary exercise training increases host butyrate concentration and its bacterial genera, which is associated with an increase in fat-free mass in early life [52].
It is believed that an increase in butyrate levels after exercise protects against intestinal inflammation and colon cancer [53, 54]. The mechanism of these changes is not yet fully understood. However, voluntary and/or forced exercise certainly influences the composition of the gut microbiota in animals.
Maternal gut microbiota during pregnancy and lactation influences the gut microbiota of rat offspring. Physical activity during pregnancy affects maternal obesity in offspring and plasma insulin and glucose concentrations [55]. Exercises started in youth can influence the bacteria ratio. In some studies, a decrease in Firmicutes and/or an increase in Bacteroidetes was observed [56, 57, 58], while other studies showed the opposite effect [49, 59, 60, 61] or no effect [62].
Early childhood exercise can influence the composition of the gut microbiota in rats and improve the development of brain function [52]. The authors confirmed the anti-inflammatory effect of regular exercise, which protects from chronic inflammatory diseases [63].
In addition, recent studies have linked the microbiota to muscle function after antibiotic use. Depletion of the microbiota by antibiotic use resulted in decreased running performance and contractile muscle function [34, 46]. A similar effect was observed with low-carbohydrate diets, which decreased SCFA production.
3.2 Associations between physical activity and changes in gut microbiota in human studies
A positive effect of physical activity on the composition of the gut microbiota has been found in human studies and confirmed animal findings. A positive effect of moderate exercise on the gut was the shortening of stool time and contact time between pathogens and the gastrointestinal mucosa [64], so exercise prevents the risk of many inflammatory diseases and various cancers. Other possible beneficial effects of moderate exercise include reduction of LPS production, increased production of SCFAs and immunoglobulins, and increase of butyrate concentration with anticarcinogenic and anti-inflammatory properties [64].
Similar to animal studies, exercise-induced changes in microbiota diversity may reduce obesity-related complications in humans. The effect on the microbiota can be assessed by measuring diversity or functions. α-diversity represents the overall diversity of samples, while β-diversity compares how different bacterial species are distributed across different samples [42].
Based on the available studies, intense exercise, compared to moderate exercise, seems to cause more significant disturbances than moderate exercise on the human body’s homeostasis [34]. High levels of inflammation (higher inflammatory interleukin-6 (IL-6)) and tumor necrosis factor-alpha (TNF-α), as well as gastrointestinal symptoms with increased intestinal permeability, were found in elite athletes [65, 66]. This may be related to diet as macronutrient intake before, during, and after exercise may influence performance and inflammatory responses in athletes [67]. Adequate carbohydrate intake after acute exercise lowers inflammatory cytokines. In addition, differences in fiber consumption impact the type and amount of SCFAs produced by microbiota [68]. Several studies have reported that fiber intake in athletes is low compared with dietary guidelines. In addition, special attention should be paid to protein supplementation in athletes. It has been demonstrated that long-term protein supplementation can have negative effects on the gut microbiota (abundance of
Importantly, the fitness status of participants also affects gut microbiota; individuals with good physical condition have more butyrate-producing bacterial taxa from the
The World Health Organization (WHO) has published recommendations for physical activity in adults (150 minutes of moderate physical activity or at least 75 minutes of vigorous physical activity per week). The composition of the gut microbiota in women who exercised according to the recommendation of WHO was modified [70]. Similarly, in male participants with insulin resistance, both high-intensity and moderate-intensity continuous exercise resulted in an increase in
A large study conducted on 86 elite rugby athletes showed a greater gut microbiota richness/diversity compared to controls [73]. This study among elite rugby players provided evidence of the beneficial effect of exercise on gut microbiota diversity. However, the results indicated that these differences between the elite and control groups were associated with dietary extremes that could represent confounding factors.
Another study on international rugby players showed differences in the composition and functional capacity of gut microbiota as well as in microbial and human-derived metabolites [74].
In addition, a positive correlation was found between cardiorespiratory fitness (CRF), an indicator of physical fitness, and microbial diversity in 39 healthy individuals, especially in taxa that augmented the production of butyrate [75]. The authors concluded that exercise can be prescribed in patients with dysbiosis-associated diseases.
The microbiota of professional and amateur cyclists was studied by Petersen [64]. They found that the gut microbiota of professional cyclists differed from that of amateurs. In addition, a correlation between certain microorganisms in professional cyclists and high training intensities was confirmed. This study suggests that training intensity influences bacterial community structure.
Higher exercise intensity leads to changes in the gut microbiota (Figure 1). Exercise leads to a positive change in the bacterial composition of the gut microbiota. Higher exercise intensities require dietary intervention to prevent gastrointestinal dysfunction and inflammatory responses. Longitudinal studies monitoring exercise intensity, diet and other characteristics, and gut microbiota are still lacking. To express the intensity level of physical activity, the rate of energy expenditure expressed as metabolic equivalents (METs) is used: 1 MET is the rate of energy expenditure at rest, which for most people approximates an oxygen uptake of 3.5 milliliters per kilogram of body weight per minute (Figure 1).
Figure 1.
Exercise can increase the number of beneficial microbial species and enrich the diversity of microflora.
Murtaza and coworkers [76] investigated the effects of different nutritional protocols on the fecal microbiota of elite endurance race walkers during an intense training program. This study showed that an intense training load with different dietary patterns had effects on the diversity of the gut microbiota. Specifically, it was found that a ketogenic, low-carbohydrate, and high-fat diet resulted in changes in the richness of some bacterial species [76].
Furthermore, the health benefits of physical activity in older adults have been established in several scientific studies. A relationship between physical activity and the diversity of the intestinal microbiota has been found in elderly people [77]. The abundance of
Overall, physical activity could be a strong modulator of gut microbiota composition. Experimental data showed that physical activity between 60 and 70% VO2max affected β diversity; interestingly, exercise at 70% VO2max resulted in an increase of α diversity or a decrease in
Further studies need to clarify the effects of different types, intensities, and frequencies of physical activity on microbiota diversity and function. High intensity of physical activity decreases producers of SCFAs and increases pathogenic bacteria. This condition requires dietary supplementation [59] or a nutritional strategy [1] to maintain the structure and richness of the gut microbiota.
4. The beneficial effect of probiotics in physically active individuals
Probiotics are currently defined as live microorganisms that have a beneficial health effect on the host when consumed in adequate amounts [81, 82]. They have an impact on the intestinal ecosystem through interactions with the host cells as well as intestinal microbiota regulating gut mucosal immunity. Among others, these interactions can contribute to improving the intestinal microenvironment, strengthening the intestinal barrier, modulating mucus secretion and the secretion of immunoglobulins or cytokines, as well as activating the innate immune response.
The beneficial role of probiotics relies on their ability to modulate the host’s microbiota and to improve the barrier function of the gut mucosa [83, 84]. Probiotics produce broad-spectrum inhibitory bacteriocins and metabolites such as SCFAs inducing a decrease of the pH less favorable for bacterial growth [85]. Higher SCFA concentrations also reduce the differentiation of dendritic cells, thus decreasing pro-inflammatory cytokines production [86, 87, 88].
Probiotics improve the barrier function and tight junctions (TJs) between intestinal epithelial cells at the level of signaling pathways leading to the increase of the mucus layer or to the production of defensins as well as proteins of TJs. They regulate the expression of the TJs, where cellular contacts occur and thus maintain cell morphology. As have already been reviewed, several probiotic strains, like
Other important components that build a protective barrier and avoid the adhesion of harmful bacteria to the epithelial cells are the mucus layer and cells of the intestinal epithelium and underlying lamina propria [90]. Each of them consists of several cell types preventing any direct contact with bacteria in the intestinal lumen. The intestinal epithelium consists of enterocytes responsible for absorbing molecules from the intestinal lumen. Paneth cells specialized in synthesizing and secreting antimicrobial peptides (AMPs) upon contact with enteric bacteria, Goblet cells, and entero-endocrine cells [90, 91, 92]. Goblet cells produce mucus and are mainly composed of high molecular weight glycoproteins called mucins. They are of two types: secreted mucins are responsible for the formation of the mucus layer, while transmembrane mucins are likely involved in signaling pathways [93, 94, 95]. A healthy mucus layer plays an important role in preventing inflammatory and infectious diseases. Altered expression of specific mucins was associated with gastrointestinal diseases such as Crohn’s disease [96] and ulcerative colitis [97] highlighting the importance of these proteins in the intestine. Several studies confirmed that specific strains of probiotic bacteria might affect the mucus barrier by regulating mucin expression. Thus, they can influence the properties of the mucus layer and indirectly regulate the gut immune system [89]. In multiple
Recent findings demonstrate that probiotics modulate the intestinal immune system by activating the immune response by recognizing specific receptors of innate immunity cells (epithelial cells, dendritic cells, and T cells). These receptors are called pattern recognition receptors (PRR) and include mostly Toll-like receptors (TLRs) and nucleotide-binding oligomerization domain agents (NODs) [105]. They are recognized by MAMPs (microbe-associated molecular patterns). Their interaction with the gut epithelium stimulates the cells of the gut immune system at the lamina propria [106]. Differentiation of T helper lymphocytes and the activation of regulatory T cells stimulate the pro- or anti-inflammatory cytokines production. Probiotic bacteria, especially various
Several studies have shown that probiotics supplementation could improve immune function in athletes [109]; reduce upper respiratory tract illness (URTI) [110], gastrointestinal symptoms [111, 112, 113], and gut permeability [114, 115]; as well as increase physical performance in elite and competitive athletes [113, 116].
Existing studies have shown an association between intestinal microbiota composition and physical activity, suggesting that modifications in the gut microbiota composition may contribute to the physical performance and exercise capacity of the host [117]. Probiotics may promote health through the improvement of the immune system and indirectly influence the performance of athletes by preventing illnesses that negatively affect healthy training [109, 118]. Recently, the International Society of Sports Nutrition (ISSN) provided a position stand on probiotics, concluding that probiotics have strain-specific effects in athletes [119]. Specific probiotic strains can improve the integrity of the gut barrier function in athletes after prolonged exercise, especially in the heat, which has been shown to increase gut permeability potentially causing systemic toxemia. Administration of selected probiotic strains has been linked to improved body composition and lean body mass, improved recovery from muscle-damaging exercise, normalizing age-related declines in testosterone levels, reductions in cortisol levels indicating improved responses to a physical or mental stressor, reduction of exercise-induced lactate, and increased neurotransmitter synthesis, cognition, and mood [reviewed in 119].
Generally, mid to long-term benefits (supplementation periods varying from 2 weeks to 3 months) of probiotics on physical performance have been studied [117]. In different studies, various probiotic strains and doses were examined, so it is difficult to compare the obtained results. Among them, the most studied bacteria are members of
In male runners, supplementation with a multi-strain probiotic (
Probiotic supplementation (
Probiotics, belonging to the
In mice, oral administration of either
However, not all studies have shown enhancements in endurance performance following probiotic use in highly trained subjects or athletes [119]. It has been shown that the exhaustive endurance exercise was not affected in endurance-trained males after 4 weeks of
Multi-strain probiotic supplementation (
Multi-strain probiotic supplementation for 12 weeks, combined with circuit training, improved muscular performance to a similar degree as circuit training alone in healthy, sedentary males [138], confirming the positive effect of resistance training on muscular outcomes, demonstrated well by other probiotic and exercise interventions among athletes [136, 137].
The well-established probiotic effects on gut health and immune system function may benefit endurance athletes, who perform high-intensity training and often encounter physiological challenges associated with GI and immune health during and after a competition. However, high-quality clinical studies, with adequate power, is necessary to uncover the impacts of probiotics on physical performance and the mechanisms of action through which probiotics affect exercise outcomes.
5. Conclusions
In recent years, the research of human gut microbiota and their interaction with their human host has extensively increased. It has been shown that the composition of the gut microbiota is influenced by several factors such as diet, age, host genetics, drugs, as well as exercise and its level of activity. Animal and human studies have indicated that gut microbiota plays an important role in the occurrence of several diseases. Mainly, it has been evidenced that its composition and function have a direct effect on host physiology and can also affect physical performance.
Exercise improves the diversity of the gut microbiota, the maintenance of normal gut physiology, and contributes to the reduction of gastrointestinal symptoms and inflammatory markers in various pathological conditions as well as altering hundreds of metabolites.
Therefore, regular physical activity should be considered as a treatment to maintain the eubiosis of the microbiota, leading to an improvement in health status. Higher CRF levels lead to greater bacterial diversity, regardless of diet. Aerobic activities appear to be able to produce significant changes in the composition of the microbiota, although the modalities and intensity of exercise may affect the microbiota differently.
The amount and frequency recommended by WHO (the minimum dose of physical activity) for adults seem to cause some changes in the composition of the microbiota. Strenuous and/or excessively prolonged exercise with inadequate carbohydrate intake may have a negative impact on the microbiota due to inflammation and gastrointestinal symptoms. Nevertheless, further studies are needed to understand how physical activity and diet independently affect the microbiota.
The use of probiotics has recently received increasing attention. Probiotics have potential health benefits, generally improving or restoring the gut microbiota, and have been shown to modulate the immune system. Recent studies have shown that probiotics reduce upper respiratory tract illness (URTI) and the onset and severity of gastrointestinal symptoms as well as gut barrier function impairment during intense exercise. By improving the immune system, they indirectly influence the performance of athletes by preventing diseases that negatively affect healthy exercise. Through SCFAs produced by probiotic bacteria, they contribute to improved energy production and reduce inflammation in the gut of physically active individuals. Selected probiotic strains have been associated with improved body composition and lean body mass, improved recovery from muscle-damaging exercise, normalization of age-related decline in testosterone levels, and reduction in cortisol levels and exercise-induced lactate. The use of probiotics is a promising approach to improve the health, well-being, and performance of athletes.
Conflict of interest
The author has no competing interest to declare that may directly or indirectly affect the content of this article.
Appendices and nomenclature
antimicrobial peptides | |
cardiorespiratory fitness | |
intraepithelial lymphocytes | |
interferon gamma | |
interleukin-6 | |
international society of sports nutrition | |
lipopolysaccharide | |
microbe-associated molecular patterns | |
metabolic equivalents | |
nucleotide-binding oligomerization domain agents | |
short-chain fatty acids | |
tight junctions | |
toll-like receptors | |
tumor necrosis factor-alpha | |
upper respiratory tract illness | |
world health organization |
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