Ruiqi Hu1
Shuwei Li1,2
Hui Diao1,2Chongbo Huang1,2Jiayou Yan1,2Xiaolan Wei1,2Mengjia Zhou1,2Peng He1,2Tianwei Wang1,2Hongsen Fu1Chengbo Zhong1Chi Mao1Yongsheng Wang1Shengyao Kuang1,2
Wenjie Tang1,2*- 1Livestock and Poultry Biological Products Key Laboratory of Sichuan Province, Sichuan Animtech Feed Co., Ltd, Chengdu, Sichuan, China
- 2Animal Breeding and Genetics Key Laboratory of Sichuan Province, Sichuan Animal Science Academy, Chengdu, Sichuan, China
Intestinal health is closely associated with overall animal health and performance and, consequently, influences the production efficiency and profit in feed and animal production systems. The gastrointestinal tract (GIT) is the main site of the nutrient digestive process and the largest immune organ in the host, and the gut microbiota colonizing the GIT plays a key role in maintaining intestinal health. Dietary fiber (DF) is a key factor in maintaining normal intestinal function. The biological functioning of DF is mainly achieved by microbial fermentation, which occurs mainly in the distal small and large intestine. Short-chain fatty acids (SCFAs), the main class of microbial fermentation metabolites, are the main energy supply for intestinal cells. SCFAs help to maintain normal intestinal function, induce immunomodulatory effects to prevent inflammation and microbial infection, and are vital for the maintenance of homeostasis. Moreover, because of its distinct characteristics (e.g. solubility), DF is able to alter the composition of the gut microbiota. Therefore, understanding the role that DF plays in modulating gut microbiota, and how it influences intestinal health, is essential. This review gives an overview of DF and its microbial fermentation process, and investigates the effect of DF on the alteration of gut microbiota composition in pigs. The effects of interaction between DF and the gut microbiota, particularly as they relate to SCFA production, on intestinal health are also illustrated.
1. Introduction
The gastrointestinal tracts (GITs) of mammals are home to abundant microorganism communities. As the largest interface between internal and external environments, the GIT is the habitat of the greatest number and diversity of microorganisms. It has been estimated that pig gut contains approximately 110 species of microorganisms, across 40 families and nine phyla (1). These microorganisms, including their genomes and extrachromosomal elements, interact with the host environment and are defined as gut microbiota (2–5). The ecosystem of the gut microbiota is complex and dynamic, and is involved in a symbiotic relationship with the host environment (6). Moreover, it plays a critical role in maintaining a healthy gut environment, further affecting nutrient utilization and physiological and immune function in the pig intestine (7, 8).
The gut microbiota composition of pigs varies and depends on GIT segment and pig age, sex, and diet, etc. It was reported that, in pigs from 11 to 12 weeks of age, the microbiota in the ileum was dominated by members of Bacillota, accounting for 90% of bacteria. In the cecum and colon, the proportion of Bacteroidota started to grow and accounted for approximately 40% to 60% of bacteria (9, 10). Apart from influencing the internal function of pigs, diet is also able to influence gut microbiota composition during the nutrient utilization process. Within the diet, dietary fiber (DF) supplementation plays a key role in influencing the composition of the gut microbiota, depending on its type, origins, and physicochemical properties, mainly because it escapes the digestive process in the small intestine and becomes available for microbial fermentation when it enters the distal ileum and colon (11, 12).
Although DF is not efficiently digested by enzymes, it is an integral part of the pig diet because it is a source of energy and has beneficial effects on intestinal health. The products of microbial fermentation of DF, short-chain fatty acids (SCFAs), are the main energy source of intestinal cells and maintain intestinal health and immune function (13). The benefits of DF and its fermentative metabolites on intestinal health drive new insights in the search for alternative strategies to antibiotic growth promoters (AGPs), which was initiated because of the ban on antibiotics issued in animal and feed systems worldwide (14). The objective of this review is to discuss the impact of DF on pig gut microbiota alteration, and of SCFA-mediated regulation on intestinal functioning and immunity. The conclusion will emphasize the importance of the interactive effects between DF and gut microbiota in influencing intestinal health and host health and performance.
2. Dietary fiber
A comprehensive understanding of DF has been developed thus far, with extensive studies conducted mostly in relation to the effects of DF on nutrient digestion, physiological and immune function, and intestinal health, depending on various DF characteristics (13, 15, 16). DF can be defined in various ways. Generally, DF represents the sum of carbohydrates that are undigestible by endogenous enzymes, namely non-starch polysaccharides (NSPs) and lignin (13, 16). These carbohydrates are mainly naturally present in plant cell wall components, including cellulose, hemicellulose, and pectin. Some non-cell wall components, such as resistant starch and some non-digestible oligosaccharides, possess effects comparable to those of NSP and lignin, and can therefore also be categorized as DFs (16). Common feedstuffs rich in fiber content include oats, wheat, barley, and by-products such as cereal hulls and distiller’s dried grains with solubles (DDGS) (13). The composition and physicochemical properties of DF vary widely in different feedstuffs and, consequently, have distinct functions in nutrient digestive processes. The composition of DF in different feedstuffs/crops is listed in Table 1. The major concern about DF, associated with its role in nutrient digestive processes, is related to its low energy value and negative effects on nutrient digestibility, which can also vary by DF characteristics. Despite its adverse effects on nutrient utilization, however, DF should be included in the diet at a minimum level to maintain normal physiological function and intestinal health. This section will provide a general introduction to DF to better understand the interaction between DF and the gut microbiota.
Table 1 Composition of DF commonly used in feedstuffs/crops*.
2.1. Classification of dietary fibers
DF can be classified according to its constituents, type of oligosaccharides/polysaccharides, physicochemical properties, and physiological role in digestion. However, these classification methods do not completely cover all fiber categories (17), and, generally, the most accepted classification of DF is based on its solubility and fermentability. Fibers are classified into two categories in terms of solubility: soluble and insoluble fibers. The chemical structure of DF, and its interaction with water molecules, determines its degree of solubility. The insoluble fraction includes cellulose, part of hemi-cellulose, and lignin, forming a linear and ordered crystalline structure in the solution. Fiber sources containing a large insoluble fraction commonly utilized in swine diets include wheat bran, soybean hull, oat hulls, and DDGS, which are mainly plant co-products. The structure of soluble fractions, i.e., pectin, gum, and β-glucan, is highly branched, contributing to the increased solubility of DF (18). DFs with different degrees of solubility have different impacts on nutrient digestive processes and microbial fermentation metabolism (12, 15). It has been reported that soluble fibers are, generally, fermentable, whereas insoluble fibers are hardly fermented. Some soluble fibers are viscous, such as pectin, galactomannan, β-glucan, and psyllium, and others, including fructooligosaccharides (FOSs) and inulin, are non-viscous. Owing to their insolubility in water, insoluble fibers do not form gels and have little association with viscosity (19, 20).
2.2. Physicochemical properties
DF has different impacts on gut physiological function, largely associated with its physicochemical properties, i.e., solubility, viscosity, and water-holding/bonding properties (21). It has been found that insoluble NSPs (e.g., wheat bran) increased the average daily feed intake (ADFI) of weaned piglets by decreasing the mean retention time (MRT) of digesta along the GIT, whereas soluble NSPs (i.e., pectin and sugar beet pulp) tended to prolong the digesta MRT and increase satiety, consequently reducing the piglets’ feed intake (22, 23). Fermentation of soluble fibers starts in the ileum, whereas insoluble fibers are hardly fermented until entering the hindgut. Compared with insoluble fibers, soluble fibers are more easily degraded by microbial enzymes, contributing to higher levels of fermentation (24). Karr-Lilienthal et al. found that wheat bran containing a large insoluble fiber fraction resulted in poor fiber fermentation compared with sugar beet pulp with a high pectin content and soybean hull containing a high soluble fraction (25, 26). Moreover, soluble fibers can increase the viscosity of digesta in the small intestine (18). Thus, the viscosities of pectin and β-glucan are generally higher than that of cellulose in pig diets (27). Viscous fiber can bind water, leading to increased viscosity and modified digesta transit time. Thus, viscosity is an important factor affecting nutrient digestibility (28, 29). In addition, viscosity is likely to influence microbial fermentation by affecting colonic cells, a key source of energy, although it is not a dominant contributor to energy absorption (13). Fibers with low and high viscosities contributed to slow and rapid fermentation and SCFA production, respectively, by variably affecting digesta transit (30). Furthermore, DF combines with water to form a colloidal suspension, which is known as the water-holding capacity (31). Water-holding capacity, to some extent, determines swelling, that is, the solubilization and dispersion by the surrounding water of the DF structure (32). It has been shown that high fermentability is associated with high solubility, swelling, and water-holding capacity (33). Moreover, DF expansion and dispersion lead to easier access to microbial enzymes and promote fiber fermentation and SCFA production (34). In conclusion, it is critical to understand the physicochemical properties of DF, as they shed light on the mechanisms of DF that affect the physiological function of pig intestines.
2.3. Alterative to AGPs
DFs have been regarded as a potential alternative to antibiotic growth promoters (AGPs) since the use of AGPs has been banned or restricted in several countries (13). AGPs are efficient tools that increase the efficiency of transforming feed into animal products, and improve animal health and performance (35). However, the problem of increased resistance to bacteria of animal origin has been a great concern for human health throughout the world (35). Shang et al. have reported that DF can reduce diarrhea in postweaning pigs and improve their intestinal health by modulating the gut microbiota (36). Moreover, the metabolites of DF fermentation, especially butyrate, have been shown to benefit mucosa growth and increase water reabsorption in the large intestine by stimulating sodium absorption (37). Thus, rapidly fermented fibers, e.g., sugar beet pulp, might exert an anti-diarrheal effect (38). In addition, the use of DFs in the place of AGPs largely mitigates concerns related to the economic costs of producing the latter, particularly when antibiotics are also required for therapeutic or health-promoting purposes. Plant-derived compounds, such as tannins, are playing a cost-effective role in animal nutrition and leading to the development of a more demanding market (39). Overall, DF can be an effective alternative to AGPs because it positively modulates the gut environment and promotes the growth of beneficial bacteria, consequently improves pig health.
3. DF fermentation
Unlike ruminants, in which extensive fermentation occurs in the rumen, in monogastric animals, nearly all DFs escape the digestive process in the stomach and small intestine and pass into the colon, which is the major site of fermentation (13, 40). Studies have also found that substantial fermentation occurs in the distal ileum, where certain species of bacteria reside (14). Before fermentation starts, polysaccharides are broken down into smaller forms, or into monosaccharides, by microbial hydrolytic enzymes in a depolymerization process (13, 41). The rate of depolymerization largely determines how quickly carbohydrates become available for microbial fermentation (13). In addition, the degree of fermentability is associated with the physicochemical properties of the DF, that is, its solubility, water-holding capacity, and viscosity (41). Highly branched DF has been shown to have a larger surface area, which makes it more readily digestible by microbial enzymes, and, therefore, is more rapidly fermented (42).
The end products of DF fermentation (i.e., SCFAs) are considered the main energy sources of intestinal cells, and promote immune function and maintain intestinal health. The major site of SCFA absorption is the large intestine, where approximately 90% of SCFAs are metabolized (41). Acetates, propionate, and butyrate are the SCFAs most discussed when investigating microbial fermentation metabolites. The production of these major fermentation metabolites through microbial fermentation is illustrated in Figure 1. Acetate is the most abundant SCFA, accounting for approximately 90% of total SCFAs (13). Butyrate plays key roles in the proliferation of mucosal epithelial cells, and in strengthening the intestinal barrier, and is regarded as the main energy source for colonic cells (43). Butyrate can be synthesized by acetate and lactate when utilized by specific bacteria (44). Furthermore, the concentration of SCFAs varies along the GIT, with a lower SCFA concentration present from the cecum to the distal colon (45). A low amount of propionate was reported because most propionate is metabolized in the liver (46). Acetate was reported to be the most abundant SCFA in peripheral circulation, and to mediate the glucose metabolism and fatty acids utilization in skeletal muscle (47). The fiber fermentation process, and SCFA metabolism pathways, are reported and illustrated well in the study by Jha and Berrocoso (13).
Figure 1 Microbial fermentation process and SCFA production.
Various studies have revealed that distinct DF characteristics can affect SCFA outcomes. A higher soluble fraction leads to an increased SCFA concentration in the small intestine, as soluble fibers are easily fermentable. Insoluble fibers, however, are fermented in the more distal parts of the GIT (48). Bai et al. observed that a higher concentration of acetate was produced by the microbial fermentation of xylan and xylooligosaccharide, whereas propionate and butyrate were produced in higher concentrations by the microbial fermentation of β-glucan and inulin (49); Ellner et al. conducted a study to compare the production of SCFAs when pigs were fed rye and rapeseed meal, and when they were fed wheat and soybean meal. The results showed that rye and rapeseed meal led to higher concentrations of SCFAs in the pigs’ jejunums and colons (50).
In conclusion, through DF fermentation, SCFAs are released as an energy source and help to maintain intestinal health. Fermentability and SCFA production largely depend on DF physical structures and chemical properties. DF fermentation enables the interaction between DFs and gut microbiota, which will be reviewed in the next section.
4. DF-microbiota interaction and intestinal health
4.1. Gut microbiota in pigs
In monogastric animals, three phyla, Bacillota, Bacteroidota, and Pseudomonadota, generally accounting for over 1,000 species of bacteria, predominate (13, 51). The species of bacteria colonizing the GIT vary in different gut segments. Zhao et al. analyzed the microbial population in four gut segments of matured pigs. They found that the predominant genera in the small intestine were aerobes, or facultative bacteria, whereas in the large intestine, the majority of the bacterial population were anaerobes. Pseudomonadota and Bacillota were the predominant phyla in the jejunum and ileum, and accounted for 70% and 20% of the total population, respectively. In turn, in the cecum and colon, Bacillota was the predominant phylum (> 75%), and Pseudomonadota accounted for approximately 13% of the total population (52). In general, the predominant bacteria along the GIT are Streptococcus, Eubacterium, Lactobacillus, Clostridium, and Propionibacterium (10). The gut microbiota profile in pigs is related to multiple factors, including their age, breed, health status, and diet. For newborn piglets, microbiota colonization mainly depends on their exposure to bacteria, including the sow and the gut environment. Escherichia coli and Streptococcus spp. are the initial colonizers, creating an anaerobic environment that favors the growth of Bacteroides, Bifidobacterium, Clostridium, and Lactobacillus. Lactobacillus dominates the microbiota profile because of its beneficial effect in inhibiting colonization by pathogens (53, 54). There is a dramatic alteration in the gut microbiota composition of weaning piglets when a new cereal-based diet is introduced, and this leads to the gut microbiota profile can becoming more specific, as it has been shown that Prevotella is more abundant and has a higher growth rate (55).
Fibers are broken down by microbiota and fermented into SCFAs for host utilization. DF acts as a substrate in the fermentation process and contributes to selective microbiota proliferation, resulting in the alteration of gut microbiota composition. The section below gives an in-depth overview of the alteration of microbiota composition affected by DF in terms of related studies in recent years. Furthermore, the factors involved in the DF–microbiota interaction will be discussed.
4.2. Effect of DF on microbiota composition
During the continuous digestion process of nutrients, a decreased amount of digesta flow enters the distal part of the GIT, leading to the alteration of fermentation metabolites and microbiota composition (56). Bacteria colonizing different GIT segments have been shown to have spatial heterogeneities that exert distinct effects on host health. It should be noted that the benefits derived from colonized bacteria are a result of the contributions of the whole microbiota community, rather than the effect of a single species (13). Spatial heterogeneity can be ascribed to different nutrient supplies for microbiota colonization in different segments (30, 57). Various studies have reported that the alteration of gut microbiota can be largely attributed to different DF characteristics. Generally, DF promotes the growth of bacteria species that are more capable of fermenting fibers than other species. In addition, a probable mechanism by which fibers can alter gut microbiota composition is that DF causes retained digesta; thus, more time is available for the proliferation of selective microbiota (13).
Wu et al. observed that Bacteroidota and Turicibacter were more abundant with increased crude fiber content in both the cecum and jejunum of growing pigs when soybean was the main fiber source (58); Ellner et al. also found a higher abundance of Bacteroidota in the colons of growing pigs fed with rapeseed meal (RSM) than in those fed with soybean meal (SBM) (50). This might be explained by the greater insolubility of an RSM-based diet, contributing to the growth of Bacteroidota, which in turn has been shown to increase with increased contents of resistant starch and maize bran, both of which contain large insoluble fractions (59). Moreover, there is evidence that a higher abundance of Bacteroidota is associated with weight loss (59, 60). In the study of Ellner et al., pigs fed an RSM-based diet were observed with reduced weight gain and higher abundance of Bacteroidota (58). Conversely, Luo et al. found a lower abundance of Bacteroidota in the colons of weaning pigs with increased galactose in the diet content when using pectin as the main fiber source. This might be explained by the high viscosity of pectin, leading to damage to the mucosal surface, thus modulating colonic morphology and bacterial colonization (61).
Heinritz et al. observed a higher abundance of Lactobacillus in the hindguts of growing pigs fed on diets containing a high content of NDF, which was similar to the results of Chen, Loo, and Heinritz (62–64), whereas it was observed that a lower abundance of lactobacilli in the ileum was associated with increased galactose (65). Chen et al. found higher abundances of Lactobacillus and bifidobacteria in the ileum and colon, respectively, with increased NDF content, in pigs fed wheat bran and pea fiber diets than in those fed a soybean fiber diet. Lower E. coli abundance was also observed in the ileum of pigs that were fed the wheat bran diet than in those fed the soybean fiber diet. The results showed that increasing DF modulates the gut microbiota, possibly in a pattern of promoting the growth of beneficial bacteria (i.e., Lactobacillus and bifidobacteria), and suppresses the growth of pathogenic bacteria (i.e., E. coli) (66).
Thus, those fiber-degrading species associated with the particular physicochemical properties of targeting fibers can also affect bacterial colonization. For instance, actinobacteria and Bacteroidota are both common insoluble DF-degrading species, and their presence affects the performance and health of their hosts. It has been shown that an increased ratio of Bacillota-to-Bacteroidota reduces the incidence of diarrhea and infections (57). The results of recent studies related to the effect of different fibers on the alteration of gut microbiota composition of pigs at different growth stages are shown in Table 2.
Table 2 Results of studies investigating the effect of fiber on alternation of gut microbiota composition.
The effect of DF on the alteration of gut microbiota composition is associated with fermentation metabolites, particularly SCFAs (Figure 2). Higher abundances of actinobacteria, and Bacillota or Fibrobacteres, could promote butyrate production, as Bacillota and actinobacteria are the dominant bacteria that produce butyrate (68). Heinritz et al. observed a positive correlation between acetate and butyrate production and colonic bifidobacteria and Lactobacillus. Moreover, decreased enterobacteria in feces and increased production of butyrate in the colon were observed with the addition of wheat bran to pigs’ diets (62). SCFA production influences pigs’ physiological and immune functioning; thus, the variation in individual SCFA concentrations due to distinct degrees of DF fermentation could provide insights into improving pig health and performance. Therefore, the gut microbiota varies depending on the pig life stage and GIT segment, displaying a spatially heterogeneous phenomenon. Bacteria exhibit substrate preference toward specific fiber characteristics, regulating the gut microbiota composition by promoting the growth of bacteria that are more capable of fermenting specific fibers. This resulted in the further variation in SCFA concentrations.
Figure 2 An example of gut microbiota alteration facilitated by the microbial fermentation of DF.
4.3. Health-promoted effect of DF via gut microbiota manipulation
The gut microbiota community is composed of a specific ratio of various bacterial species, in which species alternately restrict each other’s function and depend on each other to create an ecological balance. An imbalance in the microbiota community causes gut dysbiosis, which contributes to the development of diseases in pigs, including respiratory infection (73), postweaning diarrhea (74), impairment of the gut–liver axis (75), and intestinal barrier dysfunction (76). The fact that DF can alter microbiota composition indicates that the gut microbiota can be manipulated by DF as a way of improving the health of pigs. It has been reported that insufficient DF intake disturbs the microbiota community, leading to the damage of mucosal layers and increased pathogen susceptibility (77). Wang et al. observed that DF deprivation caused the consistent extinction of Bifidobacterium and Lactobacillus, and decreased SCFA concentration in pig ileum and feces, whereas xylan supplementation extenuated dysbiosis by selectively promoting the growth of Bifidobacterium pseudocatenulatum in the large intestine. Moreover, a positive correlation was observed between SCFA concentration and B. pseudocatenulatum abundance (63), indicating that the restoration of dysbiosis is induced by DF deprivation. Onarma et al. have investigated the beneficial effects of a high-fiber rapeseed diet by replacing soybean meal (SBM) with rapeseed meal (RSF). The authors found that RSF favored the growth of beneficial bacteria, including Lachnospira and Coprococcus, and suppressed the growth of opportunistic pathogenic bacteria, suggesting that RSF has an anti-inflammatory effect and that it reduces the risk of dysbiosis in weaned pigs (78). Therefore, DF can act as a bioactive compound to exert a regulative effect on gut microbiota by attenuating dysbiosis, promoting or depressing specific microbial abundances, and normalizing the gut environment.
4.4. A Hierarchical view of fiber specificity related to microbiota accessibility
Fibers with high specificity can be accessed and fermented by only a restricted number of bacteria, resulting in the promotion of specific bacterial growths, regardless of the environmental condition (79). Rogers et al. observed the response of Bacteroides thetaiotaomicron in the human gut to 12 carbohydrates to investigate its utilization preference. The results showed that certain carbohydrates were prioritized in the utilization process of B. thetaiotaomicron (80). Moreover, the selective accessibility and utilization of bacteria for specific fibers enables bacterial growth. In terms of this fiber specificity, a hierarchical view has been proposed to classify fibers as either low hierarchy or high hierarchy. Low-hierarchy fibers, such as inulin, can be accessed and fermented by a number of bacterial species (79). Thus, competition is present among bacterial species in the fermentation process, depending on their ability to ferment fibers. In the case of high-hierarchy fibers, which generally contain a high insoluble fraction, a limited number of bacteria can access and effectively ferment them. DFs are classified as high hierarchy, mostly because of their complex physicochemical structure, that is, their insoluble matrices and linkage and branch types (81, 82). In general, the more complex the structures are, the fewer bacteria can access and ferment them. This can be explained by the physical property, that is, their degree of insolubility, which can hinder the accessibility and fiber degradation by enzymes (83). Complete saccharification becomes more difficult when many microbial enzymes are required, because of their complex chemical structure. Among high-hierarchy fibers, competition was much less severe, and the promotion of target bacterial growth was more pronounced than that of low-hierarchy fibers (79).
5. DF–microbiota interaction and intestinal health
Intestinal health is determined by a combination of factors, including diet supplementation, mucosa integrity, gut microbiota, and the immune system (13). Metabolites derived from microbial fermentation can be considered a result of the interaction between DF supplementation and gut microbiota, and play a critical role in facilitating intestinal health. In this section, we will primarily discuss the effects of SCFAs on intestinal health.
5.1. Maintenance of intestinal integrity and barrier function
SCFAs produced by microbial fermentation of specific DFs result in distinct functions on host health. Cellulose present in oat hulls can produce SCFAs to improve nutrient digestibility and intestinal integrity, and modulate gut microbiota (14). SCFAs, particularly butyrate, produced in the hindgut, can meet 60%–70% of the energy requirements for colonic cells and are largely absorbed in weaning and growing pigs (84, 85). The efficient utilization of energy enabled by SCFAs requires the normal function of the intestinal mucosa, largely depending on the colonic cells that exert the main function. Therefore, the function of SCFAs is closely associated with intestinal mucosa integrity. SCFAs can regulate colonic cell proliferation and growth, thus maintain normal absorption and metabolism functions (85). Furthermore, SCFAs, particularly butyrate, are crucial in enhancing intestinal barrier function, which acts as the first line of defense against pathogens (13). Maintaining the intestinal physical barrier is achieved by promoting global cell differentiation and mucin-related gene expression (86, 87), and enhancing mucus excretion and thickness (88).
5.2. Enhancement of immune function and prevention of inflammation
The potential mechanism of the anti-inflammatory effect of DF is associated with the gut microbiota and microbiota-derived SCFAs. For instance, it has been reported that DF was involved in addressing inflammatory colonic damage, possibly via the activity of acetate, which may play a role in the regulation of neutrophil recruitment, as shown in an experimental model of colitis (89). SCFAs enhance immune function by interacting with immune cells, such as enterocytes, dendritic cells, and helper T cells, consequently affecting adaptive immunity and the inflammatory response (84). In turn, SCFAs facilitate the development of leukocytes and decrease colonic pH, which favor the growth of beneficial bacteria that produce SCFAs (90). Fang et al. found that supplementation with 1 g/kg sodium butyrate in the diet can lower the incidence of diarrhea in pigs and boost their immunity after weaning. This can be explained by the fact that sodium butyrate mitigates weaning stress by increasing the serum IgG concentration and the IgA+ cell population in the distal small intestine, and maintains mucosal integrity (91). The mRNA expression levels of tight junction proteins associated with wound healing in the intestine were found to be increased by sodium butyrate supplementation in the diet (92). Furthermore, it was found that SCFAs initiate innate immune responses when exposed to preadipocytes, implying that the presence of SCFAs is beneficial to immune modulation during inflammation. To prevent excessive inflammation, SCFAs promote the differentiation of regulatory T cells that can suppress effector T-cell function and increase IL-10 production (93). Thus, SCFAs could play an essential role in the maintenance of a healthy intestine by regulating immune responses and preventing inflammation.
5.3. Immunomodulatory effect in microbial infection
A variety of studies have demonstrated the immunomodulatory role of SCFAs in bacterial infections (94) (95). It was found that acetate could enhance the innate immune response to Clostridium difficile by interacting with neutrophils and innate lymphoid cells (96); furthermore, hosts infected with C. difficile were detected to have lower levels of butyrate-producing bacteria (97). An increase in butyrate concentrations diminishes C. difficile colonization, suggesting that butyrate has an effective role to play in the prevention of bacterial infections (97, 98). The rate of butyrate-producing bacteria in fecal samples was found to decrease under inflammatory bowel disease (IBD) (99). When IBD occurs, intestinal macrophages are largely replaced by monocyte cells circulating in the blood (99, 100). These monocytes eventually achieve maturation in the intestinal lamina propria and obtain bactericidal properties. Butyrate was reported to promote bactericidal properties by stimulating the metabolic shifts of macrophages, and initiating the production of antimicrobial peptides to increase bactericidal activity (100). Studies conducted on human subjects showed that butyrate could act as an anti-inflammatory factor by suppressing nuclear factor kappa B (NF-κB) and interferon gamma (IFN-γ). NF-κB signaling pathways are crucial to the immune response against microbial pathogens, as they are involved in the transcriptional modulation of cytokines, that is, tumor necrosis factor alpha (TNF-α), which actively interacts with the prevention of microbial activity in infections such as Mycobacterium tuberculosis (101). Furthermore, feeding fibers is an effective way to enrich the SCFA-producing bacterial population via extensive microbial fermentation. Overall, SCFAs have been shown to be indirectly involved in immunomodulation via molecular pathways and cellular processes to control and reduce the severity of microbial infection, suggesting the vital role of SCFAs in host−pathogen interactions.
5.4. DF, gut microbiota, and intestinal pathology
GIT impairments, including constipation, drooling, dysphagia, and gastroparesis, have been reported in Parkinson’s disease (PD) in humans (102–104). Emerging studies have observed gut microbiota alterations in patients with PD. For instance, Akkermansia and Lactobacillus were increased (105, 106), and Prevotella and Faecalibacterium were decreased (105, 106) in PD patients. Prevotella and Faecalibacterium are SCFA-producing bacteria species; hence, their decreased presence decreases SCFA concentration in PD patients (107). This implies that there is a potential correlation between gut microbiota alteration and intestinal pathology that further impacts SCFA production. Bishehsari et al. found that colon polyposis was associated with gut microbiota dysbiosis, characterized by decreased SCFAs and bacteria, in a rat model. High-fiber supplements have been regarded as an effective treatment, leading to increased SCFA concentrations, and, therefore, a reduction in the severity of symptoms associated with polyposis (108). The protection against colon carcinogenesis could be explained by the fact that DF exhibits a prebiotic effect and favors the growth of beneficial bacteria. Furthermore, increased SCFA production has been reported to modulate cancerous epithelial cells, and exert anti-inflammatory effects in the colon (108). Therefore, existing evidence has revealed the interplay between DF, gut microbiota, and intestinal pathology, and has shown that fermentation metabolites can act as regulatory compounds in the intestinal pathological process.
5.5. Maintenance of an anaerobic environment
Microbial fermentation is a process in which the gut environment shifts from being aerobic to anaerobic. SCFAs, particularly butyrate, play key roles in maintaining the gut anaerobic environment and gut homeostasis. During dysbiosis in the gut environment, DF supplementation provides an opportunity for anaerobic bacteria to use fermentative substrates to produce butyrate (13). In homeostatic situations, intestinal tissues utilize butyrate as an energy source through β-oxidation, a process of consuming oxygen, contributing to the maintenance of an anaerobic environment (109, 110). Alternatively, intestinal cells gain energy by anaerobic glycolysis, which can increase the oxygen concentration in the gut environment, resulting in the proliferation of harmful facultative bacteria, such as Salmonella (110).
6. Concluding remarks
In this review, we addressed recent findings regarding different DFs’ alteration of the gut microbiota profile. The components and physicochemical properties of DF, such as solubility, have been an important factor affecting fiber-degrading bacterial growth, and, consequently, influencing host performance and health. This results in distinct SCFA production, which plays a vital role in influencing intestinal health, since SCFAs maintain normal intestinal function, participate in immune regulation against inflammation and microbial infection, and maintain gut homeostasis. A variety of studies have demonstrated the beneficial effect of DF, namely its promotion of SCFA-producing bacteria, which in turn promotes intestinal health and pig health and performance. This supportive evidence has driven us to gain new insight into proper fiber selection when it is associated with different pig life stages and health statuses to optimize the gut microbiota profile. However, the adverse effects of fibers, such as their anti-nutritional effects, binding toxins, and reduction of nutrient digestibility, should also be taken into consideration. Relevant future research could emphasize DF supply from the perspective of optimizing the gut microbiota profile, thus improving DF feeding strategies in future practice.
Author contributions
RH conceived and designed the entire review, and wrote the draft. HD, WT, JY, XW, MZ, PH, TW, HF, CZ, CM, YW, and SK reviewed and edited the draft. All authors contributed to the article and approved the submitted version.
Funding
The present study was financially supported by the Sichuan Science and Technology Programmes (2021JDYZ0001, 2021ZDZX0009).
Conflict of interest
Authors RH, SL, HD, CH, JY, XW, MZ, PH, TW, HF, CZ, CM, YW, SK and WT were employed by company Animtech Feed Co., Ltd.
Publisher’s note
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Keywords: gut microbiota, dietary fiber (DF), microbial fermentation, short-chain fatty acids (SCFAs), intestinal health
Citation: Hu R, Li S, Diao H, Huang C, Yan J, Wei X, Zhou M, He P, Wang T, Fu H, Zhong C, Mao C, Wang Y, Kuang S and Tang W (2023) The interaction between dietary fiber and gut microbiota, and its effect on pig intestinal health. Front. Immunol. 14:1095740. doi: 10.3389/fimmu.2023.1095740
Received: 11 November 2022; Accepted: 16 January 2023;
Published: 14 February 2023.
Edited by:
Ming Jiang, Guangdong Academy of Agricultural Sciences, ChinaReviewed by:
Tarique Hussain, Nuclear Institute for Agriculture and Biology, PakistanZhiru Tang, Southwest University, China
Xiangfeng Kong, Institute of Subtropical Agriculture (CAS), China
Copyright © 2023 Hu, Li, Diao, Huang, Yan, Wei, Zhou, He, Wang, Fu, Zhong, Mao, Wang, Kuang and Tang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Wenjie Tang, wenhan28@126.com