SCFA; gut microbiota; inflammatory responses; pectin; pig; Microbiology; Microbiology (medical)
Abstract :
[en] As pectin is widely used as a food and feed additive due to its tremendous prebiotic potentials for gut health. Yet, the underlying mechanisms associated with its protective effect remain unclear. Twenty-four piglets (Yorkshire × Landrace, 6.77 ± 0.92 kg) were randomly divided into three groups with eight replicates per treatment: (1) Control group (CON), (2) Lipopolysaccharide-challenged group (LPS), (3) Pectin-LPS group (PECL). Piglets were administrated with LPS or saline on d14 and 21 of the experiment. Piglets in each group were fed with corn-soybean meal diets containing 5% citrus pectin or 5% microcrystalline cellulose. Our result showed that pectin alleviated the morphological damage features by restoring the goblet numbers which the pig induced by LPS in the cecum. Besides, compared with the LPS group, pectin supplementation elevated the mRNA expression of tight junction protein [Claudin-1, Claudin-4, and zonula occludens-1 (ZO-1)], mucin (Muc-2), and anti-inflammatory cytokines [interleukin 10 (IL-10), and IL-22]. Whereas pectin downregulated the expression of proinflammatory cytokines (IL-1β, IL-6, IL-18), tumor necrosis factor-&alpha (TNF-α), and NF-κB. What is more, pectin supplementation also significantly increased the abundance of beneficial bacteria (Lactobacillus, Clostridium_sensu_stricto_1, Blautia, and Subdoligranulum), and significantly reduced the abundance of harmful bacteria, such as Streptococcus. Additionally, pectin restored the amount of short-chain fatty acids (SCFAs) after being decreased by LPS (mainly Acetic acid, Propionic acid, and Butyric acid) to alleviate gut injury and improve gut immunity via activating relative receptors (GPR43, GPR109, AhR). Mantel test and correlation analysis also revealed associations between intestinal microbiota and intestinal morphology, and intestinal inflammation in piglets. Taken together, dietary pectin supplementation enhances the gut barrier and improves immunity to ameliorate LPS-induced injury by optimizing gut microbiota and their metabolites.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Dang, Guoqi ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Wang, Wenxing; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Zhong, Ruqing; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Wu, Weida; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Chen, Liang; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Language :
English
Title :
Pectin supplement alleviates gut injury potentially through improving gut microbiota community in piglets.
NSCF - National Natural Science Foundation of China
Funding text :
This work was supported by National Natural Science Foundation of China (NSFC; 31802072).DG acknowledges the China Scholarship Council (CSC NO. 202103250006).
Adamberg K. Adamberg S. Ernits K. Larionova A. Voor T. Jaagura M. et al. (2018). Composition and metabolism of fecal microbiota from normal and overweight children are differentially affected by melibiose, raffinose and raffinose-derived fructans. Anaerobe. 52, 100–110. doi: 10.1016/j.anaerobe.2018.06.009, PMID: 29935270
Bjerrum L. E. R. M. Leser T. D. et al. (2006). Microbial community composition of the ileum and cecum of broiler chickens as revealed by molecular and culture-based techniques. Poult. Sci. 85, 1151–1164. doi: 10.1093/ps/85.7.1151, PMID: 16830854
Borisova M. A. Achasova K. M. Morozova K. N. Andreyeva E. N. Litvinova E. A. Ogienko A. A. et al. (2020). Mucin-2 knockout is a model of intercellular junction defects, mitochondrial damage and ATP depletion in the intestinal epithelium. Sci. Rep. 1:21135. doi: 10.1038/s41598-020-78141-4
Canfora E. E. Meex R. C. R. Venema K. Blaak E. E. (2019). Gut microbial metabolites in obesity, NAFLD and T2DM. Nat. Rev. Endocrinol. 5, 261–273. doi: 10.1038/s41574-019-0156-z
Carvalho C. M. Gross L. A. de Azevedo M. J. Viana L. V. (2019). Dietary fiber intake (supplemental or dietary pattern rich in fiber) and diabetic kidney disease: a systematic review of clinical trials. Nutrients 11:347. doi: 10.3390/nu11020347
Chen T. Chen D. Tian G. Zheng P. Mao X. Yu J. et al. (2020). Effects of soluble and insoluble dietary fiber supplementation on growth performance, nutrient digestibility, intestinal microbe and barrier function in weaning piglet. Anim. Feed Sci. Techol. 260:114335. doi: 10.1016/j.anifeedsci.2019.114335
Chen S. Zhou Y. Chen Y. Gu J. (2018). Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 17, i884–i890. doi: 10.1093/bioinformatics/bty560
Dang G. Wu W. Zhang H. Everaert N. (2021). A new paradigm for a new simple chemical: butyrate & immune regulation. Food Funct. 24, 12181–12193. doi: 10.1039/d1fo02116h
Das T. Jayasudha R. Chakravarthy S. Prashanthi G. S. Bhargava A. Tyagi M. et al. (2021). Alterations in the gut bacterial microbiome in people with type 2 diabetes mellitus and diabetic retinopathy. Sci. Rep. 1:2738. doi: 10.1038/s41598-021-82538-0
den Besten G. van Eunen K. Groen A. K. Venema K. Reijngoud D. J. Bakker B. M. (2013). The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 9, 2325–2340. doi: 10.1194/jlr.R036012
Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998. doi: 10.1038/nmeth.2604, PMID: 23955772
Gavin P. G. Mullaney J. A. Loo D. Cao K. L. Gottlieb P. A. Hill M. M. et al. (2018). Intestinal Metaproteomics reveals host-microbiota interactions in subjects at risk for type 1 diabetes. Diabetes Care 10, 2178–2186. doi: 10.2337/dc18-0777
Gonzalez-Sole F. Sola-Oriol D. Ramayo-Caldas Y. Rodriguez-Prado M. Gonzalez Ortiz G. Bedford M. R. et al. (2022). Supplementation of xylo-oligosaccharides to suckling piglets promotes the growth of fiber-degrading gut bacterial populations during the lactation and nursery periods. Sci. Rep. 1:11594. doi: 10.1038/s41598-022-15963-4
Guan Z. W. Yu E. Z. Feng Q. (2021). Soluble dietary fiber, one of the Most important nutrients for the gut microbiota. Molecules 22:6802. doi: 10.3390/molecules26226802
He J. Han S. Li X. X. Wang Q. Q. Cui Y. Chen Y. et al. (2019). Diethyl Blechnic exhibits anti-inflammatory and Antioxidative activity via the TLR4/MyD88 signaling pathway in LPS-stimulated RAW264.7 cells. Molecules 24:4502. doi: 10.3390/molecules24244502, PMID: 31835323
He X. Q. Liu D. Liu H. Y. Wu D. T. Li H. B. Zhang X. S. et al. (2022). Prevention of ulcerative colitis in mice by sweet tea (Lithocarpus litseifolius) via the regulation of gut microbiota and butyric-acid-mediated anti-inflammatory signaling. Nutrients 11. doi: 10.3390/nu14112208
Holman D. B. Gzyl K. E. Mou K. T. Allen H. K. (2021). Weaning age and its effect on the development of the swine gut microbiome and Resistome. Msystems. 6:e0068221. doi: 10.1128/mSystems.00682-21, PMID: 34812652
Holmstrom K. Collins M. D. Moller T. Falsen E. Lawson P. A. (2004). Subdoligranulum variabile gen. nov., sp. nov. from human feces. Anaerobe 3, 197–203. doi: 10.1016/j.anaerobe.2004.01.004
Horiuchi H. Kamikado K. Aoki R. Suganuma N. Nishijima T. Nakatani A. et al. (2020). Bifidobacterium animalis subsp. lactis GCL2505 modulates host energy metabolism via the short-chain fatty acid receptor GPR43. Sci. Rep. 1:4158. doi: 10.1038/s41598-020-60984-6
Hua M. Liu Z. Sha J. Li S. Dong L. Sun Y. (2021). Effects of ginseng soluble dietary fiber on serum antioxidant status, immune factor levels and cecal health in healthy rats. Food Chem. 365:130641. doi: 10.1016/j.foodchem.2021.130641
Huang S. M. Wu Z. H. Li T. T. Liu C. Han D. D. Tao S. Y. et al. (2020). Perturbation of the lipid metabolism and intestinal inflammation in growing pigs with low birth weight is associated with the alterations of gut microbiota. Sci. Total Environ. 719:137382. doi: 10.1016/j.scitotenv.2020.137382
Hughes E. R. Winter M. G. Duerkop B. A. Spiga L. Furtado de Carvalho T. Zhu W. et al. (2017). Microbial respiration and Formate oxidation as metabolic signatures of inflammation-associated Dysbiosis. Cell Host Microbe 2, 208–219. doi: 10.1016/j.chom.2017.01.005
Kim H. J. Kim D. Kim K. W. Lee S. H. Jang A. (2021). Comparative analysis of the gut microbiota of mice fed a diet supplemented with raw and cooked beef loin powder. Sci. Rep. 1:11489. doi: 10.1038/s41598-021-90461-7
Kiros T. G. Luise D. Derakhshani H. Petri R. Trevisi P. D’Inca R. et al. (2019). Effect of live yeast Saccharomyces cerevisiae supplementation on the performance and cecum microbial profile of suckling piglets. PLoS One 7:e0219557. doi: 10.1371/journal.pone.0219557
Koh A. De Vadder F. Kovatcheva-Datchary P. Bäckhed F. (2016). From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cells 6, 1332–1345. doi: 10.1016/j.cell.2016.05.041
Konda P. Y. Poondla V. Jaiswal K. K. Dasari S. Uyyala R. Surtineni V. P. et al. (2020). Pathophysiology of high fat diet induced obesity: impact of probiotic banana juice on obesity associated complications and hepatosteatosis. Sci. Rep. 1:16894. doi: 10.1038/s41598-020-73670-4
Lee M. Chang E. B. (2021). Inflammatory bowel diseases (IBD) and the microbiome-searching the crime scene for clues. Gastroenterology 2, 524–537. doi: 10.1053/j.gastro.2020.09.056
Li Y. J. Chen X. Kwan T. K. Loh Y. W. Singer J. Liu Y. et al. (2020). Dietary fiber protects against diabetic nephropathy through short-chain fatty acid-mediated activation of G protein-coupled receptors GPR43 and GPR109A. J. Am. Soc. Nephrol. 6, 1267–1281. doi: 10.1681/ASN.2019101029
Louis P. Flint H. J. (2009). Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 1, 1–8. doi: 10.1111/j.1574-6968.2009.01514.x
Lu Y. Yuan H. Zuo X. Chang Y. Li X. (2021). Biomethane yield, physicochemical structures, and microbial community characteristics of corn Stover pretreated by urea combined with mild temperature Hydrotherm. Polymers (Basel). 13:2207. doi: 10.3390/polym13132207, PMID: 34279351
Lynch S. V. Pedersen O. (2016). The human intestinal microbiome in health and disease. N. Engl. J. Med. 24, 2369–2379. doi: 10.1056/NEJMra1600266
Magoc T. Salzberg S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 21, 2957–2963. doi: 10.1093/bioinformatics/btr507
Nevara G. A. Muhammad S. K. S. Zawawi N. Mustapha N. A. Karim R. (2021). Dietary fiber: fractionation, characterization and potential sources from defatted oilseeds. Foods. 10:754. doi: 10.3390/foods10040754
Niu Q. Li P. Hao S. Zhang Y. Kim S. W. Li H. et al. (2015). Dynamic distribution of the gut microbiota and the relationship with apparent crude fiber digestibility and growth stages in pigs. Sci. Rep. 5:9938. doi: 10.1038/srep09938
Ozato N. Saito S. Yamaguchi T. Katashima M. Tokuda I. Sawada K. et al. (2019). Blautia genus associated with visceral fat accumulation in adults 20-76 years of age. NPJ Biofilms Microbiom. 1:28. doi: 10.1038/s41522-019-0101-x
Qin P. Zou Y. Dai Y. Luo G. Zhang X. Xiao L. (2019). Characterization a novel butyric acid-producing bacterium Collinsella aerofaciens Subsp Shenzhenensis Subsp. Nov. Microorganisms. 3:78. doi: 10.3390/microorganisms7030078
Reyman M. van Houten M. A. van Baarle D. Bosch A. Man W. H. Chu M. et al. (2019). Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat. Commun. 1:4997. doi: 10.1038/s41467-019-13014-7
Sarkar A. Mandal S. (2016). Bifidobacteria-insight into clinical outcomes and mechanisms of its probiotic action. Microbiol. Res. 192, 159–171. doi: 10.1016/j.micres.2016.07.001
Sharma A. Akagi K. Pattavina B. Wilson K. A. Nelson C. Watson M. et al. (2020). Musashi expression in intestinal stem cells attenuates radiation-induced decline in intestinal permeability and survival in drosophila. Sci. Rep. 1:19080. doi: 10.1038/s41598-020-75867-z
Sun X. Cui Y. Su Y. Gao Z. Diao X. Li J. (2021). Dietary fiber ameliorates lipopolysaccharide-induced intestinal barrier function damage in piglets by modulation of intestinal microbiome. Msystems 6, e01374–01320. doi: 10.1128/mSystems.01374-20
Tang S. Chen Y. Deng F. Yan X. Zhong R. Meng Q. et al. (2022). Xylooligosaccharide-mediated gut microbiota enhances gut barrier and modulates gut immunity associated with alterations of biological processes in a pig model. Carbohydr. Polym. 294:119776. doi: 10.1016/j.carbpol.2022.119776
Tang S. Zhong R. Yin C. Su D. Xie J. Chen L. et al. (2021). Exposure to high aerial ammonia causes hindgut Dysbiotic microbiota and alterations of microbiota-derived metabolites in growing pigs. Front. Nutr. 8:689818. doi: 10.3389/fnut.2021.689818
Usuda H. Okamoto T. Wada K. (2021). Leaky gut: effect of dietary fiber and fats on microbiome and intestinal barrier. Int. J. Mol. Sci. 14:7613. doi: 10.3390/ijms22147613
Wan F. Wang M. Zhong R. Chen L. Han H. Liu L. et al. (2021). Supplementation with Chinese medicinal plant extracts from Lonicera hypoglauca and Scutellaria baicalensis mitigates colonic inflammation by regulating oxidative stress and gut microbiota in a colitis mouse model. Front. Cell. Infect. Microbiol. 11:798052. doi: 10.3389/fcimb.2021.798052
Wang Q. Garrity G. M. Tiedje J. M. Cole J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 16, 5261–5267. doi: 10.1128/AEM.00062-07
Wang J. Ji H. Wang S. Liu H. Zhang W. Zhang D. et al. (2018). Probiotic lactobacillus plantarum promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Front. Microbiol. 9:1953. doi: 10.3389/fmicb.2018.01953
Wang X. Wang W. Wang L. Yu C. Zhang G. Zhu H. et al. (2019). Lentinan modulates intestinal microbiota and enhances barrier integrity in a piglet model challenged with lipopolysaccharide. Food Funct. 1, 479–489. doi: 10.1039/c8fo02438c
Wen X. Zhong R. Dang G. Xia B. Wu W. Tang S. et al. (2022). Pectin supplementation ameliorates intestinal epithelial barrier function damage by modulating intestinal microbiota in lipopolysaccharide-challenged piglets. J. Nutr. Biochem. 109:109107. doi: 10.1016/j.jnutbio.2022.109107
Wu J. Wang K. Wang X. Pang Y. Jiang C. (2021). The role of the gut microbiome and its metabolites in metabolic diseases. Protein Cell 5, 360–373. doi: 10.1007/s13238-020-00814-7
Wu W. Zhang L. Xia B. Tang S. Xie J. Zhang H. (2020). Modulation of pectin on mucosal innate immune function in pigs mediated by gut microbiota. Microorganisms. 4:535. doi: 10.3390/microorganisms8040535
Xia B. Wu W. Zhang L. Wen X. Xie J. Zhang H. (2021). Gut microbiota mediates the effects of inulin on enhancing sulfomucin production and mucosal barrier function in a pig model. Food Funct. 21, 10967–10982. doi: 10.1039/d1fo02582a
Xiong B. Zhang W. Wu Z. Liu R. Yang C. Hui A. et al. (2021). Okra pectin relieves inflammatory response and protects damaged intestinal barrier in caerulein-induced acute pancreatic model. J. Sci. Food Agr. 3, 863–870. doi: 10.1002/jsfa.10693
Xu X. Hua H. Wang L. He P. Zhang L. Qin Q. et al. (2020). Holly polyphenols alleviate intestinal inflammation and alter microbiota composition in lipopolysaccharide-challenged pigs. Br. J. Nutr. 8, 881–891. doi: 10.1017/S0007114520000082
Yu Q. Chen X. Sun X. Li W. Liu T. Zhang X. et al. (2021). Pectic Oligogalacturonide facilitates the synthesis and activation of adiponectin to improve hepatic lipid oxidation. Mol. Nutr. Food Res. 20:e2100167. doi: 10.1002/mnfr.202100167
Zhang Y. Dong A. Xie K. Yu Y. (2018). Dietary supplementation with high fiber alleviates oxidative stress and inflammatory responses caused by severe sepsis in mice without altering microbiome diversity. Front. Physiol. 9:1929. doi: 10.3389/fphys.2018.01929
Zhou D. Pan Q. Xin F. Z. Zhang R. N. He C. X. Chen G. Y. et al. (2017). Sodium butyrate attenuates high-fat diet-induced steatohepatitis in mice by improving gut microbiota and gastrointestinal barrier. World J. Gastroenterol. 1, 60–75. doi: 10.3748/wjg.v23.i1.60
Zofou D. Shu G. L. Foba-Tendo J. Tabouguia M. O. Assob J. N. (2019). In vitro and in vivo anti-salmonella evaluation of pectin extracts and hydrolysates from “Cas mango” (Spondias dulcis) evidence based complement. Alternat. Med. 2019:3578402. doi: 10.1155/2019/3578402
Zuniga M. Monedero V. Yebra M. J. (2018). Utilization of host-derived Glycans by intestinal lactobacillus and Bifidobacterium species. Front. Microbiol. 9:1917. doi: 10.3389/fmicb.2018.01917
