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      Effects of high-altitude hypoxic environment on colonic inflammation, intestinal barrier and gut microbiota in three-way crossbred commercial pigs

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          Abstract

          In recent years, the three-way crossbred commercial pigs are extensively cultured in Tibet. However, there have been few studies about the effect of high-altitude hypoxic environment on intestinal health of them. Therefore, we selected Tibetan pigs (TP) and the three-way crossbred commercial pigs (CP-H) living in the Tibet (3,500–3,700 m in altitude) as a positive control group and treatment group, respectively. The three-way crossbred commercial pigs (CP-L) living at altitudes 800–1,000 m sea level were selected as a negative control group. The colonic chyme, colonic mucosa, colonic tissue and serum samples were collected for the detection of gut microbiota and intestinal inflammation. The results showed that high-altitude hypoxic environment promoted the occurrence of colonic inflammation, disrupted the colonic barrier to some extent. And Hematoxylin–Eosin (HE) staining revealed that mild inflammatory cell infiltration was observed in colon of CP-H. 16S rRNA gene sequencing revealed that the microbial community composition of CP-H was changed compared with CP-L. Gut bacterial communities formed distinctly different clusters in principal coordinates analysis (PCoA) space, and Chao 1 index of CP-H was also decreased. At the genus level, Terrisporobacter showed greater enrichment in the CP-H than lower-altitude pigs. Colstridium-sensu-stricto-1 showed lower enrichment in the CP-H than lower-altitude pigs. However, the concentration of valeric acid in colonic chyme of CP-H was higher than CP-L and TP. Correlation analysis indicated that Terrisporobacter was positively associated with the relative mRNA expression level of IL-1β and the content of lipopolysaccharide (LPS), and was negatively correlated with the relative mRNA expression level of IL-10. The Streptococcus was positively associated with the concentrations of valerate. In summary, high-altitude hypoxic environment changed compositions of gut microbiota, promoted the occurrence of colonic inflammation, and disrupted intestinal barrier of the three-way crossbred commercial pigs.

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          Most cited references54

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          Intestinal mucosal barrier function in health and disease.

          Mucosal surfaces are lined by epithelial cells. These cells establish a barrier between sometimes hostile external environments and the internal milieu. However, mucosae are also responsible for nutrient absorption and waste secretion, which require a selectively permeable barrier. These functions place the mucosal epithelium at the centre of interactions between the mucosal immune system and luminal contents, including dietary antigens and microbial products. Recent advances have uncovered mechanisms by which the intestinal mucosal barrier is regulated in response to physiological and immunological stimuli. Here I discuss these discoveries along with evidence that this regulation shapes mucosal immune responses in the gut and, when dysfunctional, may contribute to disease.
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            Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease.

            The intestinal tract of mammals is colonized by a large number of microorganisms including trillions of bacteria that are referred to collectively as the gut microbiota. These indigenous microorganisms have co-evolved with the host in a symbiotic relationship. In addition to metabolic benefits, symbiotic bacteria provide the host with several functions that promote immune homeostasis, immune responses, and protection against pathogen colonization. The ability of symbiotic bacteria to inhibit pathogen colonization is mediated via several mechanisms including direct killing, competition for limited nutrients, and enhancement of immune responses. Pathogens have evolved strategies to promote their replication in the presence of the gut microbiota. Perturbation of the gut microbiota structure by environmental and genetic factors increases the risk of pathogen infection, promotes the overgrowth of harmful pathobionts, and the development of inflammatory disease. Understanding the interaction of the microbiota with pathogens and the immune system will provide critical insight into the pathogenesis of disease and the development of strategies to prevent and treat inflammatory disease.
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              Bifidobacteria can protect from enteropathogenic infection through production of acetate.

              The human gut is colonized with a wide variety of microorganisms, including species, such as those belonging to the bacterial genus Bifidobacterium, that have beneficial effects on human physiology and pathology. Among the most distinctive benefits of bifidobacteria are modulation of host defence responses and protection against infectious diseases. Nevertheless, the molecular mechanisms underlying these effects have barely been elucidated. To investigate these mechanisms, we used mice associated with certain bifidobacterial strains and a simplified model of lethal infection with enterohaemorrhagic Escherichia coli O157:H7, together with an integrated 'omics' approach. Here we show that genes encoding an ATP-binding-cassette-type carbohydrate transporter present in certain bifidobacteria contribute to protecting mice against death induced by E. coli O157:H7. We found that this effect can be attributed, at least in part, to increased production of acetate and that translocation of the E. coli O157:H7 Shiga toxin from the gut lumen to the blood was inhibited. We propose that acetate produced by protective bifidobacteria improves intestinal defence mediated by epithelial cells and thereby protects the host against lethal infection.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                08 September 2022
                2022
                : 13
                : 968521
                Affiliations
                [1] 1College of Animal Science, Xinjiang Agricultural University , Urumqi, China
                [2] 2State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences , Beijing, China
                [3] 3Institute of Animal Husbandry and Veterinary Medicine, Tibet Academy of Agriculture and Animal Husbandry Science , Lhasa, China
                [4] 4Tibet Changdu Animal Husbandry General Station , Changdu, China
                Author notes

                Edited by: Zhixiong He, Institute of Subtropical Agriculture (CAS), China

                Reviewed by: Bo Zhang, China Agricultural University, China; Fanli Kong, Sichuan Agricultural University, China

                *Correspondence: Yanbin Zhu, zhuyanbin163@ 123456163.com

                These authors have contributed equally to this work

                This article was submitted to Microorganisms in Vertebrate Digestive Systems, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2022.968521
                9493363
                36160198
                bae75ea3-b947-4db9-aa41-146e34cd664e
                Copyright © 2022 Luo, Sun, Duan, Han, Zhong, Chen, Wangdui, Zhu, Wang and Zhang.

                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
                : 14 June 2022
                : 15 August 2022
                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 54, Pages: 12, Words: 7057
                Funding
                Funded by: Tibet Science and Technology
                Award ID: XZ-2019-NK-NS-003
                Funded by: Agricultural Science and Technology Innovation Program , doi 10.13039/501100012421;
                Award ID: CAAS-ZDRW202006-02
                Award ID: ASTIPIAS07
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                three-way crossbred commercial pigs,high-altitude hypoxic environment,intestinal barrier,gut microbiota,inflammatory cytokines,short-chain fatty acids

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