Physical Activity, Gut Microbiota and Gut-Brain Axis: Comparison
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Increasing evidence supports the importance of the gut microbiota (GM) in regulating multiple functions related to host physical health and, more recently, through the gut–brain axis (GBA), mental health.

Physical activity can impact significantly the gut microbiota composition and diversity, and could also produce modifications in the gut microbiota that can mediate and induce mental health benefits.

  • cognitive functions
  • anxiety
  • depression
  • microbiome
  • overweight
  • elderly
  • athletes
  • sports
  • fitness
  • overtraining

1.Introduction

In recent years, research on the interaction between gut microbiota (GM) and health has expanded considerably. High-throughput sequencing has favored and facilitated research on GM in multiple aspects [1]. Indeed, humans have specific microbial profiles at the oral, skin, reproductive organ, gastrointestinal and fecal levels [2],[3]. In particular, the human gastrointestinal (GI) tract has a microbial diversity of up to 100 trillion microorganisms, predominantly bacteria but also archaea, viruses, and parasites. The GM encodes more than three million genes that produce hundreds of metabolites [4]. Only recently, the effect of the PA on the GM has been more thoroughly investigated, although considerable difficulties persist in structuring research protocols capable of limiting the various confounding elements as much as possible. Most evidence shows that a sedentary lifestyle is associated with a higher incidence of chronic diseases [5],[6],[7], on which PA can play a preventive and therapeutic role through different mechanisms. Recently, the potential effects produced on GM have been proposed as another modality through which PA can perform beneficial functions on host health [8].

Although there is no gold standard for gut health, and its definition remains uncertain [9],[10],[11], the interaction between host PA can favor the growth of beneficial bacteria and gut cells that maintain the integrity of the intestinal surface, which acts as the first defense against pathogens. In return, the selected bacteria synthesize molecules capable of modifying the metabolism and immune functions of the host [12]. Furthermore, disruption of the gut barrier is considered one of the mechanisms of major depression and other cognitive and behavioral alterations, with the gut–brain axis (GBA) playing a role in mediating these processes [13]. In this context, PA seems able to influence this two-way communication interaction through the GBA [14].

This Hereview aims to s we summarize the current evidence about the effects that PA has on GM and how GM, in turn, can influence physical performance and cognitive functionality, providing an overview of the currently most promising aspects in this field of research. We first discuss the extent to which GM can affect the physiological condition of its host and its influence on the onset of certain pathologies when an imbalance state occurs. Next, we analyze the evidence from preclinical studies concerning different PA modalities, the effects of PA on young or elderly subjects, as well as the interaction between PA and GM-mediated physical performance and overtraining. We then review the influence of PA on the human intestinal microbiota, specifically the role of physical fitness, the impact of endurance activity, and the effect that PA can exert on the microbiota of the elderly population; lastly, we discuss the relationship between PA and GM in the overweight subjects. Finally, we look at how and to what degree PA may exert certain effects on the GBA and indirectly on cognitive function.

2.Physical Activity and Gut Microbiota in Preclinic Studies

It is now quite clear that, in animal models, exercise initiates significant changes in the GM. In agreement with Kang et al. [15], Denou et al. [16] found an increased bacterial diversity in diet-induced obesity (DIO) mice fed an high fat diet (HFD) following forced treadmill running (FTR); a proliferation of Bacteroidetes was observed in the cecum, colon, and feces with a consequent reduction in the Firmicutes:Bacteroidetes ratio. In contrast to Kang et al. [15], using a high-intensity interval training (HIIT) protocol did not result in a reduction in body mass, suggesting the possibility of different bacterial changes based on the exercise modality used. The data from this study suggest that exercise can counterbalance the changes made to the GM by obesity, but how this may occur is not entirely clear. Increased intestinal motility and reduced colonic blood flow during exercise are some of the possible modalities investigated. Ribeiro et al. [64][17] highlighted that the use of a medium-low intensity exercise (50% of maximal velocity) induces insignificant changes in the GM to counteract the effects of a prolonged HFD.

It has been found [1718] that FWR results in a significant up-regulation of the Ruminococcus gnavus species, a bacterium capable of degrading the intestinal mucosa and thus penetrating its inner and outer layers, exposing intestinal epithelial cells to immunogenic bacterial proteins and thus exacerbating intestinal inflammation [1819]. However, the regulation of mucin, the glycoprotein that makes up intestinal muscle, and the bacterial dynamics involved in relation to exercise have been little investigated. In the case of VWR, distinctive changes are induced both in the entire bacterial community and in individual taxa present in the GM of mice. Of note is the increase in the Anaerotruncus genus, a butyrate-producing bacterial group that colonizes the outer layer of the colonic mucosa and is phylogenetically related to Fecalibacterium prausnitzii, a known butyrate producer in humans [1920],[2021]. These bacteria often feed on lactate, acetate, or other intermediates produced by other bacterial strains, and so it is possible that the activity-induced changes in so-called lactate producers (e.g., lactobacilli) and butyrate producers (e.g., Anaerotruncus) are related by a cross-feeding phenomenon.

The period of life in which exercise is carried out would also appear to be important, thus representing age as a determining factor in the regulation of the GM. Indeed, Usome research has shown that the impact of GM on host physiology can be age-dependent; using ing GF mice, an early sensitive period has been identified during which the absence of an intact GM reflects physiological consequences such as the exaggerated activity of the hypothalamic-pituitary-adrenal (HPA) axis that can only be partly normalized by the introduction of Bifidobacteria infantis if administered during the early period of life [2122]. This evidence reveals that the framework of GM during development can strongly influence the health of the host throughout life. Furthermore, just as physiological systems during development are remarkably malleable and sensitive to change, likewise the GM is more plastic in the early stages of life [2223],[2324] and, consequently, the microbial ecosystem present during the early period of life may be more sensitive to environmental changes due in part to its lower stability and diversity than in adulthood. Obviously, PA ranks well among those modifiable environmental factors, and so Mika et al. [2425] hypothesize and note that exercise undertaken during early life (EL) may have a greater impact on GM than that undertaken in adulthood, corroborated recently by another study [2526]. Mika Thet al.y also [24] observe a lower species richness in juvenile than in adult rats. A similar condition was observed in humans by Yatsunenko et al. [2627], supporting the idea that it is precisely this condition of the young GM that encourages greater changes within it, unlike in the adult GM where the greater microbial complexity may make it more resistant to changes induced by environmental factors.

Li et al. [2728] note that HFDs, by reducing microbial diversity, enhancing the proliferation of a pro-inflammatory microbiota, and increasing intestinal permeability (IP), can indcan induce an increase in circulating Lipopolysaccharide (LPS) levels, endotoxins present on the membrane of certain bacteria, which are related to the onset of osteoarthritis [2829]. PA (VWR) seems able to remodel the GM by increasing its diversity and consequently reducing LPS levels in the blood and synovial fluid. According to this work, PA, in addition to reducing body weight, may have a protective effect on cartilage by modifying the GM and reducing serum LPS levels. Yuan et al. [2930] setfind out to assess the negative effects of excessive exercise on the immunity system, energy metabolism, and GM. After four weeks of the protocol (excessive ES swimming), they found GM showing a reduced α-diversity and β-diversity compared with the control group. In terms of phylum, the ES group showed an abundance of Bacteroidetes and Firmicutes at the ileocecal level and a reduction in Proteobacteria. In the families, there is a lower presence of Bacteroidales: S24-7 and Lachnospiraceae and an increase in Helicobacteraceae. At the genus level, there is an increase in Helicobater and Bacteroides and a reduction in Odoribater. It is thus observed that certain disease-related bacteria appear to be present to a greater extent in the ES group than in the control group. However, due to the limited sample, these differences do not have statistical significance.

3.Physical Activity and Gut Microbiota in Human Studies

Clarke et al. [3031] performed the first study on athletes. Expecting to find greater bacterial diversity in athletes than in sedentary subjects, they set up the study by recruiting 40 male rugby players with an average BMI of 29.1 and, due to their size, two control groups were composed of sedentary subjects, one with a BMI ≤ 25 (LBG) and the other with a BMI > 28 (HBG). Stool and blood samples were collected from all participants. Thus, greater richand greater richness and α-diversity were observed in the athletes than in the control groups, in agreement with Mörkl et al. [3132]. Microbial diversity is positively associated with protein intake, suggesting that exercise and diet are drivers of gut bacterial diversity. In the athletes’ group, an increase in butyrate-producer phylum (Firmicutes) and genus (F.prausnitzii) was observed [1920],[2021]. Furthermore, athletes and LBG show increased Akkermansiaceae family and Akkermansia genus, associated with metabolic disorders [3233]. Despite these interesting correlations between exercise and GM, the research appears confounded by its nature as a cross-sectional study and no control of confounders. Castellanos et al. [3334], using data collected through their previous observational study [3435] from a cohort of 109 volunteers (18–40 years old, BMI 20–30) identified bacterial taxa considered to be ‘key’ microorganisms for the structure of the GM since the pathogenicity of certain bacteria is not always and only related to their abundance but also to other factors such as interactions with other microorganisms. Roseburia fecis species, considered a health marker, Rikenellaceae and Erysipelotrichaceae families, whose role is not yet clear, were found in active subjects, while unclassified species of Sutterella genus, associated with impairment of cognitive and immune system function, were found in the sedentary group, suggesting that the GM of active subjects have higher efficiency. No changes were found after three weeks of HIIT protocol, indicating that short-term HIIT protocol does not impact the fecal bacterial community and that progress in the cardiorespiratory fitness (CRF) does not lead to modification of GM in the short term [3536], similarly to Moitinho-Silva [3637]. after six weeks of exercise.

Durk et al. [3738] looked for a correlation between CRF and GM composition in young (22–32 years) and healthy subjects. Although limitations like the collection of information on different variables, such as caloric intake, through subjective reports from participants, the results of this study support other supporting other similar work in both animal models and humans [3839],[3132],[1718], ifoundicating that the PA ascan be a factor that can positively affect the human GM. Bycura et al. [43][40] examined the changes in the GM following a separate double intervention for the duration of eight weeks characterized by cardiorespiratory exercise (CRE) or resistance training exercise (RTE). In contrast to contrast to Quiroga et al. [3941], where aerobic and resistance exercises were analyzed separately, observinged that only aerobic activity causes an initial significant change within the GM that subsequently decreases until it becomes irrelevant.

A first pilot study conducted by Petersen et al. [4042], on 22 professional cyclists and 11 amateurs at a competitive level, investigated whether a difference in GM composition between professionals and amateurs can be detected through an analysis of the metagenome (representative of the species present) and the metatranscriptome (representative of the functions expressed in a specific environment). There was a significant correound a significant correlation between the presence of the genus Prevotella, with concomitant upregulation of BCAAsbrain chain amino acids (BCAAs), and the time spent training (>11 h/week) in both professionals and amateurs. A decrease in Bacteroides and, among 30 cyclists, an increase in the genus Akkermansia was noted, as already observed [22][31]. It was also observed that the increased presence of Prevotella correlates with certain carbohydrate and amino acids (AAs) metabolic pathways, including the biosynthesis of BCAAs [4143]. Morishima et al. [4244] investigated the relatifonship between intensive exercise and the GM status, in female eliteund that in endurance runners (ER), compared with the non-athletic healthy control group. They found that in the ER group, , some bacteria associated with gut inflammation (Haemophilus, Rothia, and Ruminococcus ganvus) were more abundant. Counterintuitively, Fecalibacterium, known as a beneficial butyrate producer, was also more abundant in the ER group. This could be explained by the fact that an abnormal intestinal environment prompts the Fecalibacterium to produce succinate, a risk factor for diarrhea and loose stools [4345], and not butyrate. This suggests that prolonged high-intensity exercise may lead to a form of dysbiosis in the athlete.

One study [4446] attempted to assess whether endurance activity can modulate GM in elderly men and whether these changes are associated with specific cardiometabolic conditions in the host. While genus Oscillospira, associated with reduced BMI [4547],[4648], increases, species Clostridioides difficile decreases. Furthermore, changes in these taxa were correlated with changes in several cardio-metabolic risk factors such as systolic and diastolic blood pressure. Researchers found that after six months of combined training, seven high-intensity and eight moderate-intensity exercises [4749], Oscillospira, Bifidobacterium, and Anaerostipes, health-related genus [4850],[4951], were increased.

To establQuish whether a combined strength and endurance protocol canroga et al. exert[41] an effect on the GM of obese children (7–12 years), Quiroga et al. [39] pround that a combinepared a 12-week (2 × week) concurrent training protocol through which it was found that obese subjects exhibit a bacterial profile associated with this condition. Subsequently, this protocol was shown toendurance and strength training can alter GM composition and function in obese subjects by significantly reducing the phylum Proteobacteria, corroborating the results obtained by Munukka et al. [5052] and the class Gammaproteobacteria. Furthermore, an increasing trend of some bacterial genera as part of the phylum Firmicutes was observed, which made the GM of obese subjects like that of normal-weight control subjects. These results, therefore, suggest the presence of a negative bacterial profile related to the state of obesity that can be positively modified by PA. In the longest randomized controlled study to date, Kern et al. [51] set out to assess whether exercise alters the diversity, composition, and functionality of the GM in overweight or obese subjects. Specifically, the effects of regular aerobic training carried out with different modalities and intensities, but with similar energy expenditure, on the GM of 88 subjects (20–45 years old) divided into four groups: commuters traveling by non-motorized bicycles (BIKE), moderate-intensity PA (MOD) or vigorous PA (VIG) and the control group leading their usual lives (CON) are investigated over a six-month period using a specific protocol (ACTIWE) [52]. In all groups that performed PA, changes in β-diversity were observed, while low heterogeneity was found in the VIG group. In the MOD group, changes in α-diversity were noted. These discrepancies between studies may be due to the lack of a non-exercising control group and the small sample size used in previous studies. 

4.Physical Activity, Gut Microbiota and Cognitive Ability

According to Gubert et al. [53], considering the concomitant intestinal dysbiosis present in several neurodegenerative diseases and the impact that PA or exercise can have on the intestinal microbiome and neuronal degeneration, a triangulation between these aspects seems plausible to assess whether PA can contribute to the modulation of neurodegeneration through GM. Among the few studies that tried to find a correlation between PA and GM in humans, none have investigated this neural aspect in-depth, whereas some studies in animal models have shown some initial evidence.

Kang et al. [15] showed that mice subjected to a 16-week training protocol reported an improvement in memory associated with the increase in the Firmicutes:Bacteroidetes ratio induced by exercise. They also poiOnt out that one hour per day of exercise can increase the relative abundance of the family Lachnospiraceae, which is negatively correlated with anxiogenic behavior and is capable of producing butyrate (SCFA), a molecule that over-regulates BDNF expression in the hippocampus and frontal cortex, supporting the survival of existing neurons and stimulating the formation of new neurons and synapses [54]. Thus, according to the authors, this association between induced changes in certain GM phyla and families and memory improvement could be used as a biomarker for exercise-induced effects at a cognitive level.

According to Gubert et al. [53], eExperimental data have shown that GM modifications induced by an aerobic activity, specifically characterized by an increase in certain bacteria (e.g., Lactobacillus plantarum and Streptococcus thermophile), are capable of inducing the synthesis of serotonin, a molecule that protects against symptoms of anxiety and depression [55]. Abraham et al. [56] extrapolated findings that seem to indicate the ability of exercise to improve cognitive function and some markers of Alzheimer’s disease (AD); using transgenic mice (APP/PS1) subjected to a 20-week treadmill exercise protocol, they note a significant improvement in the Morris Maze Test, which assesses spatial memory, and a reduction in β-amyloid plaques, one of the main aspects involved in AD [57], supporting what was previously observed by Lin et al. [58]. Near these plaques, an increase in microglia, important for brain development by providing structural and metabolic support to neurons and involved in neuroplasticity and regulation of neural repair [59], is found, underlining the neuroprotective effect of exercise. This appears to be associated with the abundance of some bacterial strains (Eubacteria, Roseburia) and the reduction of others, so these results suggest that the cognitive effects of exercise may be mediated through GM alteration, reducing the levels of microbes involved in disease exacerbation and promoting the abundance of those bacteria capable of producing SCFAs that appear beneficial.

5.Conclusion and Future Directions

Although the literature analyzing GM is steadily increasing, the effects of PA on bacterial flora remain uncertain. A PA or exercise PA performed voluntarily appears to attenuate intestinal inflammation, in contrast to a forced activity that instead increases this condition in animal models. Vigorous endurance exercise can negatively affect the GM framework in humans; furthermore, only aerobic activities can alter the GM structure, probably because of the positive correlation between CRF and microbial diversity. PA can stimulate bacterial community richness by altering SCFAs-producing species, as well as favoring the colonization of health and athletic performance-promoting strains (e.g., A. muciniphila and Veillonella). The ability to promote a bacterial composition capable of protecting the intestinal mucosa from possible permeability and counteracting HFD-induced changes in the GM is observed. Overall, PA can increase the relative abundance of phylum Bacteroidetes and reduce that of Firmicutes as well as may exert greater and more lasting benefits if undertaken from an early age, but the effects on GM seem to gradually disappear when the PA is no longer practiced. PA seems able to regPA seems able to regulate cognitive conditions (e.g., anxiety and depression) and functionality (e.g., Alzheimer’s and Parkinson’s Disease) through modifications of microbial composition and subsequently the production of certain protective molecules, to date in animal models.

Despite the promising future and interest in this research area, multiple aspects make the development of adequate study protocols complicated, first and foremost the not easy dissociation between PA and nutrition. The studies carried out on humans appear to be more difficult to interpret, first of the difficulty of dietary control also due to the instruments used for this purpose that are imprecise. Different types of bacterial genome sequencing methods and different types of PA used in the studies make it difficult to extrapolate guidelines. Future research should isolate more confounding elements, first and foremost the dietary aspect, with a greater focus on young and elderly populations, as well as on resistance training protocols where evidence is scarce. Specific attention should be paid to the development of research in humans to investigate the concrete impact of PA on the GBA.

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