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      The interaction between dietary fiber and gut microbiota, and its effect on pig intestinal health

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          Abstract

          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.

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          Most cited references110

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          Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.

          Gut commensal microbes shape the mucosal immune system by regulating the differentiation and expansion of several types of T cell. Clostridia, a dominant class of commensal microbe, can induce colonic regulatory T (Treg) cells, which have a central role in the suppression of inflammatory and allergic responses. However, the molecular mechanisms by which commensal microbes induce colonic Treg cells have been unclear. Here we show that a large bowel microbial fermentation product, butyrate, induces the differentiation of colonic Treg cells in mice. A comparative NMR-based metabolome analysis suggests that the luminal concentrations of short-chain fatty acids positively correlates with the number of Treg cells in the colon. Among short-chain fatty acids, butyrate induced the differentiation of Treg cells in vitro and in vivo, and ameliorated the development of colitis induced by adoptive transfer of CD4(+) CD45RB(hi) T cells in Rag1(-/-) mice. Treatment of naive T cells under the Treg-cell-polarizing conditions with butyrate enhanced histone H3 acetylation in the promoter and conserved non-coding sequence regions of the Foxp3 locus, suggesting a possible mechanism for how microbial-derived butyrate regulates the differentiation of Treg cells. Our findings provide new insight into the mechanisms by which host-microbe interactions establish immunological homeostasis in the gut.
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            A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility.

            Despite the accepted health benefits of consuming dietary fiber, little is known about the mechanisms by which fiber deprivation impacts the gut microbiota and alters disease risk. Using a gnotobiotic mouse model, in which animals were colonized with a synthetic human gut microbiota composed of fully sequenced commensal bacteria, we elucidated the functional interactions between dietary fiber, the gut microbiota, and the colonic mucus barrier, which serves as a primary defense against enteric pathogens. We show that during chronic or intermittent dietary fiber deficiency, the gut microbiota resorts to host-secreted mucus glycoproteins as a nutrient source, leading to erosion of the colonic mucus barrier. Dietary fiber deprivation, together with a fiber-deprived, mucus-eroding microbiota, promotes greater epithelial access and lethal colitis by the mucosal pathogen, Citrobacter rodentium. Our work reveals intricate pathways linking diet, the gut microbiome, and intestinal barrier dysfunction, which could be exploited to improve health using dietary therapeutics.
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              Short chain fatty acids and gut microbiota differ between patients with Parkinson's disease and age-matched controls.

              Patients with Parkinson's disease (PD) frequently have gastrointestinal symptoms (e.g. constipation) and exhibit the PD-typical pathohistology in the enteric nervous system (ENS). Both, clinical symptoms and pathohistological changes in the ENS occur at early stages and can precede the motor manifestations of PD. Two recent studies reported an association between changes in gut microbiota composition and PD. We hypothesized that alterations in gut microbiota might be accompanied by altered concentrations of short chain fatty acids (SCFA), one main metabolic product of gut bacteria.
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                Author and article information

                Contributors
                Journal
                Front Immunol
                Front Immunol
                Front. Immunol.
                Frontiers in Immunology
                Frontiers Media S.A.
                1664-3224
                14 February 2023
                2023
                : 14
                : 1095740
                Affiliations
                [1] 1 Livestock and Poultry Biological Products Key Laboratory of Sichuan Province, Sichuan Animtech Feed Co., Ltd , Chengdu, Sichuan, China
                [2] 2 Animal Breeding and Genetics Key Laboratory of Sichuan Province, Sichuan Animal Science Academy , Chengdu, Sichuan, China
                Author notes

                Edited by: Ming Jiang, Guangdong Academy of Agricultural Sciences, China

                Reviewed by: Tarique Hussain, Nuclear Institute for Agriculture and Biology, Pakistan; Zhiru Tang, Southwest University, China; Xiangfeng Kong, Institute of Subtropical Agriculture (CAS), China

                *Correspondence: Wenjie Tang, wenhan28@ 123456126.com

                This article was submitted to Nutritional Immunology, a section of the journal Frontiers in Immunology

                Article
                10.3389/fimmu.2023.1095740
                9972974
                36865557
                d0b83f93-62a1-44a6-99b4-7748acf5ec3b
                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.

                History
                : 11 November 2022
                : 16 January 2023
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 110, Pages: 11, Words: 6067
                Funding
                The present study was financially supported by the Sichuan Science and Technology Programmes (2021JDYZ0001, 2021ZDZX0009).
                Categories
                Immunology
                Review

                Immunology
                gut microbiota,dietary fiber (df),microbial fermentation,short-chain fatty acids (scfas),intestinal health

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