Xylooligosaccharide-mediated gut microbiota enhances gut barrier and modulates gut immunity associated with alterations of biological processes in a pig model.
[en] Xylooligosaccharide (XOS) has tremendous prebiotic potentials for gut health, but the relevant mechanisms are unclear. Herein, we confirmed the positive effects of dietary XOS enhancing gut barrier in a pig model via suppressing the expression of pro-inflammatory cytokines (IL-6 and IL-8). Meanwhile, XOS increased beneficial microbes Lactobacillus and decreased potential pathogenic bacteria. Moreover, XOS augmented microbiota-derived metabolites (mainly butyrate, propionate, and secondary bile acid) to strengthen the gut barrier and regulate gut immunity through activating host G-protein coupled receptors 109a or inhibiting histone deacetylases. Furthermore, XOS attenuated IgA-production and antigen cross-presentation processes. In addition, XOS supplementation led to the alteration of cell proliferation, remodeling of the energy metabolism, activation processes of serial genes or proteins, increased molecular chaperones, and the enhanced ubiquitin-proteasome pathway in cecal cells. Collectively, these results suggest that XOS enhances gut barrier and modulates gut immunity by optimizing gut microbiota and their metabolites, which is associated with alterations of biological processes.
Disciplines :
Food science Veterinary medicine & animal health
Author, co-author :
Tang, Shanlong; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China
Chen, Yuxia ; Université de Liège - ULiège > TERRA Research Centre
Deng, Fuli; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China
Yan, Xiaowei; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China
Zhong, Ruqing; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China
Meng, Qingshi; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China
Liu, Lei; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China
Zhao, Yong; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China
Zhang, Sheng; Proteomics and Metabolomics Facility, Institute of Biotechnology, Cornell University, Ithaca, NY 14853, USA
Chen, Liang; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China. Electronic address: chenliang01@caas.cn
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China. Electronic address: zhanghongfu@caas.cn
Language :
English
Title :
Xylooligosaccharide-mediated gut microbiota enhances gut barrier and modulates gut immunity associated with alterations of biological processes in a pig model.
NSCF - National Natural Science Foundation of China
Funding text :
This study was supported by the National Natural Science Foundation of China (31702119) and the Agricultural Science and Technology Innovation Program of China (CAAS-ZDRW202006-02, ASTIP-IAS07). All procedures in this study were approved by the Experimental Animal Welfare and Ethical Committee of Institute of Animal Science of Chinese Academy of Agricultural Sciences (IAS2019-34, Beijing, China).
Ang, Z., Ding, J.L., GPR41 and GPR43 in obesity and inflammation - protective or causative?. Frontiers in Immunology, 7, 2016, 28.
Bailey, M., Haverson, K., Inman, C., Harris, C., Jones, P., Corfield, G., Miller, B., Stokes, C., The development of the mucosal immune system pre- and post-weaning: Balancing regulatory and effector function. The Proceedings of the Nutrition Society 64 (2005), 451–457.
Barton, M.D., Impact of antibiotic use in the swine industry. Current Opinion in Microbiology 19 (2014), 9–15.
Berry, D., Schwab, C., Milinovich, G., Reichert, J., Ben Mahfoudh, K., Decker, T., Engel, M., Hai, B., Hainzl, E., Heider, S., Kenner, L., Muller, M., Rauch, I., Strobl, B., Wagner, M., Schleper, C., Urich, T., Loy, A., Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. The ISME Journal 6 (2012), 2091–2106.
den Besten, G., van Eunen, K., Groen, A.K., Venema, K., Reijngoud, D.J., Bakker, B.M., The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of Lipid Research 54 (2013), 2325–2340.
Beumer, J., Clevers, H., Cell fate specification and differentiation in the adult mammalian intestine. Nature Reviews. Molecular Cell Biology 22 (2021), 39–53.
Blumberg, R., Powrie, F., Microbiota, disease, and back to health: A metastable journey. Science Translational Medicine, 4, 2012, 137rv137.
Brown, K., Abbott, D.W., Uwiera, R.R.E., Inglis, G.D., Removal of the cecum affects intestinal fermentation, enteric bacterial community structure, and acute colitis in mice. Gut Microbes 9 (2018), 218–235.
Chang, P.V., Hao, L., Offermanns, S., Medzhitov, R., The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proceedings of the National Academy of Sciences of the United States of America 111 (2014), 2247–2252.
Chen, H.H., Chen, Y.K., Chang, H.C., Lin, S.Y., Immunomodulatory effects of xylooligosaccharides. Food Science and Technology Research 18 (2012), 195–199.
Chen, Y., Xie, Y., Ajuwon, K.M., Zhong, R., Li, T., Chen, L., Zhang, H., Beckers, Y., Everaert, N., Xylo-oligosaccharides, preparation and application to human and animal health: A review. Frontiers in Nutrition, 8, 2021, 731930.
Chen, Y., Xie, Y., Zhong, R., Han, H., Liu, L., Chen, L., Zhang, H., Beckers, Y., Everaert, N., Effects of graded levels of xylo-oligosaccharides on growth performance, serum parameters, intestinal morphology, and intestinal barrier function in weaned piglets. Journal of Animal Science 99 (2021), 1–8.
Chen, Y., Xie, Y., Zhong, R., Liu, L., Lin, C., Xiao, L., Chen, L., Zhang, H., Beckers, Y., Everaert, N., Effects of xylo-oligosaccharides on growth and gut microbiota as potential replacements for antibiotic in weaning piglets. Frontiers in Microbiology, 12, 2021, 641172.
Chung, H., Pamp, S.J., Hill, J.A., Surana, N.K., Edelman, S.M., Troy, E.B., Reading, N.C., Villablanca, E.J., Wang, S., Mora, J.R., Umesaki, Y., Mathis, D., Benoist, C., Relman, D.A., Kasper, D.L., Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149 (2012), 1578–1593.
Collado, M.C., Cernada, M., Bauerl, C., Vento, M., Perez-Martinez, G., Microbial ecology and host-microbiota interactions during early life stages. Gut Microbes 3 (2012), 352–365.
Cunningham, M., Azcarate-Peril, M.A., Barnard, A., Benoit, V., Grimaldi, R., Guyonnet, D., Holscher, H.D., Hunter, K., Manurung, S., Obis, D., Petrova, M.I., Steinert, R.E., Swanson, K.S., van Sinderen, D., Vulevic, J., Gibson, G.R., Shaping the future of probiotics and prebiotics. Trends in Microbiology 29 (2021), 667–685.
Fagarasan, S., Kawamoto, S., Kanagawa, O., Suzuki, K., Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annual Review of Immunology 28 (2010), 243–273.
Fang, W., Zhang, L., Meng, Q., Wu, W., Lee, Y.K., Xie, J., Zhang, H., Effects of dietary pectin on the profile and transport of intestinal bile acids in young pigs. Journal of Animal Science 96 (2018), 4743–4754.
Fei, Y., Wang, Y., Pang, Y., Wang, W., Zhu, D., Xie, M., Lan, S., Wang, Z., Xylooligosaccharide modulates gut microbiota and alleviates colonic inflammation caused by high fat diet induced obesity. Frontiers in Physiology, 10, 2019, 1601.
Flint, H.J., Scott, K.P., Louis, P., Duncan, S.H., The role of the gut microbiota in nutrition and health. Nature Reviews. Gastroenterology & Hepatology 9 (2012), 577–589.
Fu, C.Y., Li, L.Q., Yang, T., She, X., Ai, Q., Wang, Z.L., Autoinducer-2 may be a new biomarker for monitoring neonatal necrotizing enterocolitis. Frontiers in Cellular and Infection Microbiology, 10, 2020, 140.
Gao, J., Yin, J., Xu, K., Li, T., Yin, Y., What is the impact of diet on nutritional diarrhea associated with gut microbiota in weaning piglets: A system review. BioMed Research International, 2019, 2019, 6916189.
Garrett, W.S., Gordon, J.I., Glimcher, L.H., Homeostasis and inflammation in the intestine. Cell 140 (2010), 859–870.
Gevers, D., Kugathasan, S., Denson, L.A., Vazquez-Baeza, Y., Van Treuren, W., Ren, B., Schwager, E., Knights, D., Song, S.J., Yassour, M., Morgan, X.C., Kostic, A.D., Luo, C., Gonzalez, A., McDonald, D., Haberman, Y., Walters, T., Baker, S., Rosh, J., Xavier, R.J., The treatment-naive microbiome in new-onset Crohn's disease. Cell Host & Microbe 15 (2014), 382–392.
Gilad, O., Jacobsen, S., Stuer-Lauridsen, B., Pedersen, M.B., Garrigues, C., Svensson, B., Combined transcriptome and proteome analysis of bifidobacterium animalis subsp. Lactis BB-12 grown on xylo-oligosaccharides and a model of their utilization. Applied and Environmental Microbiology 76 (2010), 7285–7291.
Guo, W.L., Pan, Y.Y., Li, L., Li, T.T., Liu, B., Lv, X.C., Ethanol extract of ganoderma lucidum ameliorates lipid metabolic disorders and modulates the gut microbiota composition in high-fat diet fed rats. Food & Function 9 (2018), 3419–3431.
Heinritz, S.N., Mosenthin, R., Weiss, E., Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutrition Research Reviews 26 (2013), 191–209.
Hou, Z., Wu, D., Dai, Q., Effects of dietary xylo-oligosaccharide on growth performance, serum biochemical parameters, antioxidant function, and immunological function of nursery piglets. Revista Brasileira de Zootecnia, 49, 2020, e20190170.
Hu, C.H., Xiao, K., Luan, Z.S., Song, J., Early weaning increases intestinal permeability, alters expression of cytokine and tight junction proteins, and activates mitogen-activated protein kinases in pigs. Journal of Animal Science 91 (2013), 1094–1101.
Jacobson, A., Lam, L., Rajendram, M., Tamburini, F., Honeycutt, J., Pham, T., Van Treuren, W., Pruss, K., Stabler, S.R., Lugo, K., Bouley, D.M., Vilches-Moure, J.G., Smith, M., Sonnenburg, J.L., Bhatt, A.S., Huang, K.C., Monack, D., A gut commensal-produced metabolite mediates colonization resistance to salmonella infection. Cell Host & Microbe 24 (2018), 296–307 e297.
Kayama, H., Okumura, R., Takeda, K., Interaction between the microbiota, epithelia, and immune cells in the intestine. Annual Review of Immunology 38 (2020), 23–48.
Li, Y., Fu, X., Ma, X., Geng, S., Jiang, X., Huang, Q., Hu, C., Han, X., Intestinal microbiome-metabolome responses to essential oils in piglets. Frontiers in Microbiology, 9, 2018, 1988.
Ma, K., Saha, P.K., Chan, L., Moore, D.D., Farnesoid X receptor is essential for normal glucose homeostasis. The Journal of Clinical Investigation 116 (2006), 1102–1109.
Matamoros, S., Gras-Leguen, C., Le Vacon, F., Potel, G., de La Cochetiere, M.F., Development of intestinal microbiota in infants and its impact on health. Trends in Microbiology 21 (2013), 167–173.
Munyaka, P.M., Rabbi, M.F., Khafipour, E., Ghia, J.E., Acute dextran sulfate sodium (DSS)-induced colitis promotes gut microbial dysbiosis in mice. Journal of Basic Microbiology 56 (2016), 986–998.
Nicolas, G.R., Chang, P.V., Deciphering the chemical lexicon of host-gut microbiota interactions. Trends in Pharmacological Sciences 40 (2019), 430–445.
Nishino, K., Nishida, A., Inoue, R., Kawada, Y., Ohno, M., Sakai, S., Inatomi, O., Bamba, S., Sugimoto, M., Kawahara, M., Naito, Y., Andoh, A., Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. Journal of Gastroenterology 53 (2018), 95–106.
NRC, Nutrient requirements of swine, 11th ed, 2012, National Academies Press, Washington, DC, USA.
O'Dwyer, A.M., Lajczak, N.K., Keyes, J.A., Ward, J.B., Greene, C.M., Keely, S.J., Ursodeoxycholic acid inhibits TNFalpha-induced IL-8 release from monocytes. American Journal of Physiology. Gastrointestinal and Liver Physiology 311 (2016), G334–G341.
Oliphant, K., Allen-Vercoe, E., Macronutrient metabolism by the human gut microbiome: Major fermentation by-products and their impact on host health. Microbiome, 7, 2019, 91.
Pan, J., Yin, J., Zhang, K., Xie, P., Ding, H., Huang, X., Blachier, F., Kong, X., Dietary xylo-oligosaccharide supplementation alters gut microbial composition and activity in pigs according to age and dose. AMB Express, 9, 2019, 134.
Pang, J., Wang, S., Wang, Z., Wu, Y., Zhang, X., Pi, Y., Han, D., Zhang, S., Wang, J., Xylo-oligosaccharide alleviates salmonella induced inflammation by stimulating bifidobacterium animalis and inhibiting salmonella colonization. The FASEB Journal, 35, 2021, e21977.
Pang, J., Zhou, X., Ye, H., Wu, Y., Wang, Z., Lu, D., Wang, J., Han, D., The high level of xylooligosaccharides improves growth performance in weaned piglets by increasing antioxidant activity, enhancing immune function, and modulating gut microbiota. Frontiers in Nutrition, 8, 2021, 764556.
Pohl, C.S., Medland, J.E., Mackey, E., Edwards, L.L., Bagley, K.D., DeWilde, M.P., Williams, K.J., Moeser, A.J., Early weaning stress induces chronic functional diarrhea, intestinal barrier defects, and increased mast cell activity in a porcine model of early life adversity. Neurogastroenterology and Motility, 29, 2017, 13118.
Pourabedin, M., Guan, L., Zhao, X., Xylo-oligosaccharides and virginiamycin differentially modulate gut microbial composition in chickens. Microbiome, 3, 2015, 15.
Rivera-Chávez, F., Zhang, L.F., Faber, F., Lopez, C.A., Byndloss, M.X., Olsan, E.E., Xu, G., Velazquez, E.M., Lebrilla, C.B., Winter, S.E., Bäumler, A.J., Depletion of butyrate-producing clostridia from the gut microbiota drives an aerobic luminal expansion of salmonella. Cell Host & Microbe 19 (2016), 443–454.
Saibil, H., Chaperone machines for protein folding, unfolding and disaggregation. Nature Reviews. Molecular Cell Biology 14 (2013), 630–642.
Shang, Q., Liu, S., Liu, H., Mahfuz, S., Piao, X., Impact of sugar beet pulp and wheat bran on serum biochemical profile, inflammatory responses and gut microbiota in sows during late gestation and lactation. Journal of Animal Science and Biotechnology, 12, 2021, 54.
Smith, F., Clark, J.E., Overman, B.L., Tozel, C.C., Huang, J.H., Rivier, J.E., Blikslager, A.T., Moeser, A.J., Early weaning stress impairs development of mucosal barrier function in the porcine intestine. American Journal of Physiology. Gastrointestinal and Liver Physiology 298 (2010), G352–G363.
Taggart, A.K., Kero, J., Gan, X., Cai, T.Q., Cheng, K., Ippolito, M., Ren, N., Kaplan, R., Wu, K., Wu, T.J., Jin, L., Liaw, C., Chen, R., Richman, J., Connolly, D., Offermanns, S., Wright, S.D., Waters, M.G., (D)-beta-hydroxybutyrate inhibits adipocyte lipolysis via the nicotinic acid receptor PUMA-G. The Journal of Biological Chemistry 280 (2005), 26649–26652.
Tang, S., Zhong, R., Yin, C., Su, D., Xie, J., Chen, L., Liu, L., Zhang, H., Exposure to high aerial ammonia causes hindgut dysbiotic microbiota and alterations of microbiota-derived metabolites in growing pigs. Frontiers in Nutrition, 8, 2021, 689818.
Varshavsky, A., The ubiquitin system, autophagy, and regulated protein degradation. Annual Review of Biochemistry 86 (2017), 123–128.
Wang, Q., Wang, X.F., Xing, T., Li, J.L., Zhu, X.D., Zhang, L., Gao, F., The combined impact of xylo-oligosaccharides and gamma-irradiated astragalus polysaccharides on growth performance and intestinal mucosal barrier function of broilers. Poultry Science, 100, 2021, 100909.
Wu, J., Wang, K., Wang, X., Pang, Y., Jiang, C., The role of the gut microbiome and its metabolites in metabolic diseases. Protein & Cell 12 (2020), 360–373.
