Diversity of the human gut microbiota
Diversity and richness are among the major parameters describing the human gut microbiota. Identification of dissimilarities in microbial diversity in different populations, for example, smokers vs. nonsmokers and ill vs. healthy, is a fundamental step of microbiome studies. For instance, reduced microbial diversity is associated with various host phenotypes, such as obesity, fatty liver disease, type II diabetes, inflammatory bowel disease, to name a few. Clinical interventions (e.g., antibiotic use) and environmental factors (e.g., diet, smoking, and physical activity) also affect the microbial diversity . Accordingly, biodiversity (alpha diversity Shannon Index) parameters have been compared in athletic activity, and exercise studies. The microbial diversity was reported as unchanged regardless of the level of physical activity in five studies [15, 19, 20, 21, 25], while it was reportedly increased with increased physical activity in two studies [17, 18]. Although the diversity of gut microbiota of athletes was reported to be higher than that of nonathletes in four studies [26, 28, 29, 33]. In the current review, the diversity parameters did not respond to the stimulus of exercise in non-training individuals [44, 46, 47, 49, 50], but were affected by the training load in highly trained athletes [35, 36, 37]. Therefore, the microbial diversity does not appear to be related to the physical exercise as per se, but to the appropriate “intervention”, i.e., the time or intensity of the physical effort. These conclusions are supported by studies in the rat model conducted by Allen et al. , who showed that forced vs. voluntary training differently impacts the gut microbiota composition. In addition, Grosicki et al.  analyzed changes in the intestinal microbiota at all stages of an athlete's preparation for an ultramarathon. They observed the highest alpha-diversity values during the training periods of the lowest intensity (the preparation period and post-start period), with the lowest values reported upon an increase of the physical effort load (the pre-start period) and immediately after the physical performance, i.e., the recovery period. Furthermore, Karl et al.  showed that greater microbiota alpha diversity is not always related to gut health but may be associated with the growth of potentially harmful bacteria. This is supported by an increased abundance of the potentially pathogenic genus Veillonella [56, 57, 58, 59] in the gut of marathon runners [29, 35, 42]. Although Sheiman et al. observed an increase in Veillonella relative abundance in marathon runners post-marathon and isolated a strain of Veillonella atypica from stool samples. Inoculation of this strain into mice significantly increased exhaustive treadmill run time probably because Veillonella utilizes lactate as their sole carbon source .
Changes in Firmicutes and Bacteroidetes abundance in the gut
Firmicutes and Bacteroidetes are the two most abundant phyla that inhabit the human gut. According to some reports, these bacteria account for up to 90% of the gut microbiota [2, 61]. The Firmicutes family contains several thousand species of highly diverse bacteria. Bacteroidetes are involved in food digestion, signal transmission, gut environment control, and inhibiting the growth of undesirable microorganisms in the gut ; however, their high abundance is associated with poor microbiota with low diversity . Although, as mentioned earlier in section 4.1, high alpha diversity is not always associated with a healthy gut . Only three studies reported increased Bacteroidetes abundance after exercise [47, 49, 52]. Further, an increase in the Firmicutes/Bacteroidetes ratio is reported in six studies [16, 26, 29, 35, 36, 38], mainly among athletes. In recently reported studies, the increased ratio is associated with obesity [62, 63]. However, the increased ratio in this particular group of microbiota can be explained by efficient energy extraction from food [64, 65], which is necessary for heavy physical exertion.
Changes in SCFA producer abundance in the gut
Bacteria from the Clostridium genus are major SCFA producers. They are also involved in the pro-inflammatory immune response . An increase in the relative abundance of Clostridium genus upon physical activity was reported in two studies: one by Jang et al. , who compared the gut microbiota of body builders with that in a control group; and the other by Langsetmo et al.  in a large sample of elderly individuals. Two other studies reported a reduction in the relative abundance of Clostridium genus upon exercise intervention [47, 48]. Further, one study reported a decrease in Clostridium difficile abundance upon exercise . This bacterium is a major source of infectious diarrhea associated with toxin production in the host’s gastrointestinal tract [67, 68], especially in the elderly [69, 70, 71] and obese individuals [72, 73]. These observations suggest that moderate exercise has a positive effect on the abundance of Clostridium bacteria.
Another SCFA-producing bacterium whose relative abundance is affected by exercise is the genus Feacalibacterium and its representative Feacalibacterium prausnitzii. An increase in the population of Feacalibacterium prausnitzii was noted in relatively active individuals . Also, the population of genus Feacalibacterium was compared after a moderate exercise intervention , and in athletes versus non-training subjects [26, 27]. A decrease in its abundance was observed in professional athletes upon extreme physical exertion [36, 38]. Numerous authors have pointed out the anti-inflammatory effect of Feacalibacterium prausnitzii [74, 75], as well as of the entire Feacalibacterium genus , by associating the abundance of these bacteria with the alpha diversity of microbiota . Overall, the appraisal of available data suggests a positive effect of moderate exercise compared with that of extreme exercise.
Another SFCA producer is the genus Roseburia [78, 79]. An increase in Rosuburia genus and its representative Roseburia hominis abundance was noted in various studies when comparing an individual’s normal physical activity and upon physical exercise [15, 18, 37, 41]. A decrease in its abundance was only observed upon extreme physical exertion , confirming the previous observations of a negative effect of extreme exertion on the gut microbiota. Further, the enhanced population in the family of Lachnospiraceae or genus Lachnospira confirms the positive impact of moderate-intensity exercise on the gut microbiota [21, 22, 26, 36, 41, 47].
Another important SCFA producer is the genus Coprococcus [80, 81]. It is associated with positive outcomes in the treatment of inflammatory bowel disease  and a reduced risk of Campylobacter infection . A marked increase or abundance of Coprococcus genus was observed in comparative studies of active vs. inactive individuals [15, 30]. Furthermore, Hampton–Marcell et al.  reported a decrease in the relative Coprococcus abundance with a decreased physical exercise in swimmers during the starting season. Interestingly enough, the Coprococcus_2 abundance tripled in runners after running a half-marathon , indicating that even extreme physical exertion can have a positive influence on the gut microbiota.
Changes in the lactic acid producer abundance in the gut
When discussing the role of gut microbiota, the lactic acid-producing bacteria from the genus Bifidobacterium and Lactobacillus, which are widely used in probiotics , must be mentioned. Their positive impact on human health is well documented . When administered as probiotics, they reduce hypercholesterolemia , improve the parameters of diabetes mellitus , and regulate local and systemic immune responses [87, 88]. Further, their decreased population has been reported in individuals with severe depression . In the context of the effects of exercise, an increase in their abundance was observed in one exercise intervention study , and in comparative studies done in athletes and non-athletes [32, 33]. By contrast, a reduction in their abundance is reported in highly trained athletes .
Other types of bacteria
Exercise affects the abundance of species from the gram-negative Prevotella genus. An increased abundance of Prevotella was noticed when comparing athletes to non-athletes [29, 33]. Moreover, the higher abundecne of Prevotella was seen during a 3300-Km row in rowers . When accompanied by a high abundance of Bacteroides and Akkermansia muciniphila, this bacterium is a marker of good intestinal health . However, that was not the case in the above studies. When not accompanied by a higher abundance of Bacteroides and Akkermansia muciniphila, Prevotella are thought to support pro-inflammatory processes , opportunistic infections, and diseases related to intestinal dysbiosis, and are proposed to be a marker of intestinal dysbiosis . These reported observations appear to confirm the negative impact of physical activity on the gut microbiota of qualified athletes.
The Ruminaceae family has been linked to a reduced intestinal permeability in 102 women . An increase in its abundance upon physical exercise has been noted in numerous studies [15, 26, 30, 33, 36, 39], both when considering different phenotypes and athletes, which indicates the positive effect of physical activity on these bacteria. Two important geniuses belong to this family: Ruminococcus, proposed by Hills et al. as a marker of intestinal dysbiosis . Ruminoccocus genus and its representative were decreased in intervention studies  and during sport preparation . The second genus that belongs to Ruminaceae family is Oscillospira, which is closely related to human health  and lean individuals [93, 94]. The abundance of Oscillospira positively correlates with microbial diversity, high-density lipoproteins, and sleep-time duration, and is inversely correlated with blood pressure, fasting glucose levels, triglycerides, and uric acid . In addition, Oscillospira abundance is reduced in Crohn’s disease and fatty liver disease. From the literature reviewed for the current systematic review, an increase in Oscillospira abundance in intervention studies was only reported by Taniguchi et al. .
Another bacterium, proposed as a new probiotic , is Akkermansia muciniphila, the main representative of the Verrucomicrobia phylum. Zhai et al. consider it as a marker of a healthy gut , which is associated with lean people . Although, its low abundance is observed in obese individuals and diabetics [97, 98]. That may be because the presence of A. muciniphila is associated with improved fat oxidation [99, 100, 101]. An increased relative A. muciniphila abundance was reported in relatively active people [15, 33] and after exercise intervention Verrucomibrobia, Verrucomicrobiaceae, Akkermansia respond , confirming the notion that moderate-intensity exercise positively affects gut health.
Exercise or physical activity may represent a strong modulator of gut microbiota composition. Moreover, the gut-muscle communication in human pathophysiology may be bidirectional, with gut microbiota representing a “cross-road” among environment, and skeletal muscle . The well-known positive health effects of exercise may be mediated by its beneficial modifications to the gut microbiota. However, when there is an exercise overload, these possible beneficial effects are overweighed by increased intestinal permeability and oxidative stress, promoting inflammation and a catabolic state that negatively impacts the functionality of skeletal muscle .
The main limitation of the current systematic review is the limited number of studies reported on this research topic. The available literature on the effects of exercise on gut microbiota is rather scanty, and only a small number of participants were analyzed in the articles included in this review. This aspect is especially evident for data on high-performance athletes.