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Effect of early antibiotic intervention on specific bacterial communities and immune parameters in the small intestine of growing pigs fed different protein level diets

Published online by Cambridge University Press:  21 May 2020

C. J. Zhang ,
M. Yu ,
Y. X. Yang ,
C. L. Mu ,
Y. Su  and
W. Y. Zhu
C. J. Zhang
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, National Center for International Research on Animal Gut Nutrition, Nanjing, Jiangsu210095, P. R. China
M. Yu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, National Center for International Research on Animal Gut Nutrition, Nanjing, Jiangsu210095, P. R. China
Y. X. Yang
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, National Center for International Research on Animal Gut Nutrition, Nanjing, Jiangsu210095, P. R. China
C. L. Mu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, National Center for International Research on Animal Gut Nutrition, Nanjing, Jiangsu210095, P. R. China
Y. Su
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, National Center for International Research on Animal Gut Nutrition, Nanjing, Jiangsu210095, P. R. China
W. Y. Zhu*
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, National Center for International Research on Animal Gut Nutrition, Nanjing, Jiangsu210095, P. R. China
*
†E-mail: [email protected]
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Abstract

Antibiotics are designed to affect gut microbiota and subsequently gut homeostasis. However, limited information exists about short- and long-term effects of early antibiotic intervention (EAI) on gut homeostasis (especially for the small intestine) of pigs following antibiotic withdrawal. We investigated the impact of EAI on specific bacterial communities, microbial metabolites and mucosal immune parameters in the small intestine of later-growth-stage pigs fed with diets differing in CP levels. Eighteen litters of piglets were fed creep feed with or without antibiotics from day 7 to day 42. At day 42, pigs within each group were offered a normal- or low-CP diet. Five pigs per group were slaughtered at days 77 and 120. At day 77, EAI increased Enterobacteriaceae counts in the jejunum and ileum and decreased Bifidobacterium counts in the jejunum and ileum (P < 0.05). Moreover, tryptamine, putrescine, secretory immunoglobulin (Ig) A and IgG concentrations in the ileum and interleukin-10 (IL-10) mRNA and protein levels in the jejunum and ileum were decreased in pigs with EAI (P < 0.05). At day 120, EAI only suppressed Clostridium cluster XIVa counts in the jejunum and ileum (P < 0.05). These results suggest that EAI has a short-term effect on specific bacterial communities, amino acid decarboxylation and mucosal immune parameters in the small intestine (particularly in the ileum). At days 77 and 120, feeding a low-CP diet affected Bifidobacterium, Clostridium cluster IV, Clostridium cluster XIVa and Enterobacteriaceae counts in the jejunum or ileum (P < 0.05). Moreover, feeding a low-CP diet increased the concentrations of Igs in the jejunum and decreased pro-inflammatory cytokines levels in the jejunum and ileum (P < 0.05). At day 120, feeding a low-CP diet increased short-chain fatty acid concentrations, reduced ammonia and spermidine concentrations and up-regulated genes related to barrier function in the jejunum and ileum (P < 0.05). These results suggest that feeding a low-CP diet changes specific bacterial communities and intestinal metabolite concentrations and modifies mucosal immune parameters. These findings contribute to our understanding on the duration of the impact of EAI on gut homeostasis and may provide basis data for nutritional modification in young pigs after antibiotic treatment.

Keywords

antibioticlow-CP dietmicrobiotaimmune statuspigs
Type
Research Article
Information
animal , Volume 14 , Issue 10 , October 2020 , pp. 2042 - 2053
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

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References

Akdis, CA and Akdis, M 2014. Mechanisms of immune tolerance to allergens: role of IL-10 and Tregs. Journal of Clinical Investigation 124, 4678–4680.10.1172/JCI78891CrossRefGoogle ScholarPubMed
Al-Sadi, R, Boivin, M and Ma, T 2009. Mechanism of cytokine modulation of epithelial tight junction barrier. Frontiers in Bioscience-Landmark 14, 2765–2778.CrossRefGoogle ScholarPubMed
Andriamihaja, M, Davila, AM, Eklou-Lawson, M, Petit, N, Delpal, S, Allek, F, Blais, A, Delteil, C, Tome, D and Blachier, F 2010. Colon luminal content and epithelial cell morphology are markedly modified in rats fed with a high-protein diet. American Journal of Physiology Gastrointestinal and Liver Physiology 299, G1030–G1037.CrossRefGoogle ScholarPubMed
Barba-Vidal, E, Castillejos, L, Vfb, R, Cifuentes-Orjuela, G, Moreno Muñoz, JA and Martín-Orúe, SM 2017. The probiotic combination of Bifidobacterium longum subsp. Infantis CECT 7210 and Bifidobacterium animalis subsp. lactis BPL6 reduces pathogen loads and improves gut health of weaned piglets orally challenged with Salmonella typhimurium. Frontiers in Microbiology 8, 1570.CrossRefGoogle ScholarPubMed
Bordonaro, M, Lazarova, DL and Sartorelli, AC 2008. Butyrate and Wnt signaling: a possible solution to the puzzle of dietary fiber and colon cancer risk? Cell Cycle 7, 1178–1183.10.4161/cc.7.9.5818CrossRefGoogle ScholarPubMed
Brandl, K, Plitas, G, Mihu, CN, Ubeda, C, Jia, T, Fleisher, M, Schnabl, B, DeMatteo, RP and Pamer, EG 2008. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455, 804–807.CrossRefGoogle ScholarPubMed
Brandtzaeg, P 2010. The mucosal immune system and its integration with the mammary glands. The Journal of Pediatrics 156, S8–S15.10.1016/j.jpeds.2009.11.014CrossRefGoogle ScholarPubMed
Chaney, AL and Marbach, EP 1962. Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130–132.10.1093/clinchem/8.2.130CrossRefGoogle ScholarPubMed
Chomczynski, P and Sacchi, N 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate phenol chloroform extraction. Analytical Biochemistry 162, 156–159.CrossRefGoogle ScholarPubMed
Dai, ZL, Li, XL, Xi, PB, Zhang, J, Wu, G and Zhu, WY 2012. Metabolism of select amino acids in bacteria from the pig small intestine. Amino Acids 42, 1597–1608.CrossRefGoogle ScholarPubMed
Darcy-Vrillon, B, Cherbuy, C, Morel, MT, Durand, M and Duee, PH 1996. Short chain fatty acid and glucose metabolism in isolated pig colonocytes: modulation by NH4+. Molecular and Cellular Biochemistry 156, 145–151.CrossRefGoogle ScholarPubMed
Ellermann, M and Sartor, RB 2018. Intestinal bacterial biofilms modulate mucosal immune responses. Journal of Immunological Sciences 2, 13–18.Google ScholarPubMed
Fang, CL, Sun, H, Wu, J, Niu, HH and Feng, J 2014. Effects of sodium butyrate on growth performance, haematological and immunological characteristics of weanling piglets. Journal of Animal Physiology and Animal Nutrition 98, 680–685.CrossRefGoogle ScholarPubMed
Herfel, TM, Jacobi, SK, Lin, X, Jouni, ZE, Chichlowski, M, Stahl, CH and Odle, J 2013. Dietary supplementation of Bifidobacterium longum strain AH1206 increases its cecal abundance and elevates intestinal interleukin-10 expression in the neonatal piglet. Food and Chemical Toxicology 60, 116–122.CrossRefGoogle ScholarPubMed
Janczyk, P, Pieper, R, Souffrant, WB, Bimczok, D, Rothkotter, HJ and Smidt, H 2007. Parenteral long-acting amoxicillin reduces intestinal bacterial community diversity in piglets even 5 weeks after the administration. The ISME Journal 1, 180–183.10.1038/ismej.2007.29CrossRefGoogle ScholarPubMed
Jin, Y, Wu, Y, Zeng, Z, Jin, C, Wu, S, Wang, Y and Fu, Z 2016. From the cover: exposure to oral antibiotics induces gut microbiota dysbiosis associated with lipid metabolism dysfunction and low-grade inflammation in mice. Toxicological Sciences 154, 140–152.10.1093/toxsci/kfw150CrossRefGoogle ScholarPubMed
Kaiko, GE and Stappenbeck, TS 2014. Host-microbe interactions shaping the gastrointestinal environment. Trends in Immunology 35, 538–548.CrossRefGoogle ScholarPubMed
Kotunia, A, Woliński, J, Laubitz, D, Jurkowska, M, Romé, V, Guilloteau, P and Zabielski, R 2004. Effect of sodium butyrate on the small intestine development in neonatal piglets fed [correction of feed] by artificial sow. Journal of Physiology and Pharmacology 55(suppl. 2), 59–68.Google ScholarPubMed
Lange, CFMD, Pluske, J, Gong, J and Nyachoti, CM 2010. Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livestock Science 134, 124–134.CrossRefGoogle Scholar
Lawhon, SD, Russell, M, Mitsu, S and Craig, A 2010. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Molecular Microbiology 46, 1451–1464.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25, 402–408.CrossRefGoogle Scholar
Ma, X, Fan, PX, Li, LS, Qiao, SY, Zhang, GL and Li, DF 2012. Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions. Journal of Animal Science 90(suppl. 4), 266–268.CrossRefGoogle ScholarPubMed
Mu, C, Yang, Y, Luo, Z, Guan, L and Zhu, W 2016. The colonic microbiome and epithelial transcriptome are altered in rats fed a high-protein diet compared with a normal-protein diet. The Journal of Nutrition 146, 474–483.CrossRefGoogle ScholarPubMed
Mu, C, Yang, Y, Su, Y, Zoetendal, EG and Zhu, W 2017. Differences in microbiota membership along the gastrointestinal tract of piglets and their differential alterations following an early-life antibiotic intervention. Frontiers in Microbiology 8, 797.CrossRefGoogle ScholarPubMed
National Research Council (NRC) 2012. Nutrient requirements of swine, 11th revised edition. National Academy Press, Washington, DC, USA.Google Scholar
Naoki, A, Masaru, W, Hirotada, M, Shigeru, N and Hiroshi, T 2005. Identification and functional analysis of Escherichia coli cysteine desulfhydrases. Applied and Environmental Microbiology 71, 4149–4152.Google Scholar
Peng, Y, Yu, K, Mu, C, Hang, S, Che, L and Zhu, W 2017. Progressive response of large intestinal bacterial community and fermentation to the stepwise decrease of dietary crude protein level in growing pigs. Applied Microbiology and Biotechnology 4, 1–12.Google Scholar
Pieper, R, Boudry, C, Bindelle, J, Vahjen, W and Zentek, J 2014. Interaction between dietary protein content and the source of carbohydrates along the gastrointestinal tract of weaned piglets. Archives of Animal Nutrition 68, 263–280.CrossRefGoogle ScholarPubMed
Pieper, R, Kröger, S, Richter, JF, Wang, J, Martin, L, Bindelle, J, Htoo, JK, Von, SD, Vahjen, W and Zentek, J 2012. Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. The Journal of Nutrition 142, 661–667.CrossRefGoogle Scholar
Rettedal, E, Vilain, S, Lindblom, S, Lehnert, K, Scofield, C, George, S, Clay, S, Kaushik, RS, Rosa, AJ, Francis, D and Brozel, VS 2009. Alteration of the ileal microbiota of weanling piglets by the growth-promoting antibiotic chlortetracycline. Applied and Environmental Microbiology 75, 5489–5495.CrossRefGoogle ScholarPubMed
Schokker, D, Zhang, J, Vastenhouw, SA, Heilig, HG, Smidt, H, Rebel, JM and Smits, MA 2015. Long-lasting effects of early-life antibiotic treatment and routine animal handling on gut microbiota composition and immune system in pigs. PLoS ONE 10, e0116523.CrossRefGoogle ScholarPubMed
Schokker, D, Zhang, J, Zhang, LL, Vastenhouw, SA, Heilig, HG, Smidt, H, Rebel, JM and Smits, MA 2014. Early-life environmental variation affects intestinal microbiota and immune development in new-born piglets. PLoS ONE 9, e100040.CrossRefGoogle ScholarPubMed
Sukumar, K, Chattha, KS, Vlasova, AN, Gireesh, R and Saif, LJ 2014. Lactobacilli and Bifidobacteria enhance mucosal B cell responses and differentially modulate systemic antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model. Gut Microbes 5, 639–651.Google Scholar
Tedelind, S, Westberg, F, Kjerrulf, M and Vidal, A 2007. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World Journal of Gastroenterology 13, 2826–2832.CrossRefGoogle ScholarPubMed
Ushida, K, Kameue, C, Tsukahara, T, Fukuta, K and Nakanishi, N 2008. Decreasing traits of fecal immunoglobulin A in neonatal and weaning piglets. Journal of Veterinary Medical Science 70, 849–852.CrossRefGoogle ScholarPubMed
Wang, XF, Mao, SY, Liu, JH, Zhang, LL, Cheng, YF, Jin, W and Zhu, WY 2011. Effect of the gynosaponin on methane production and microbe numbers in a fungus-methanogen co-culture. Journal of Animal and Feed Sciences 20, 272–284.CrossRefGoogle Scholar
Wlodarska, M, Willing, B, Keeney, KM, Menendez, A, Bergstrom, KS, Gill, N, Russell, SL, Vallance, BA and Finlay, BB 2011. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infection and Immunity 79, 1536–1545.CrossRefGoogle ScholarPubMed
Yan, H, Potu, R, Lu, H, de Almeida, VV, Stewart, T, Ragland, D, Armstrong, A, Adeola, O, Nakatsu, CH and Ajuwon, KM 2013. Dietary fat content and fiber type modulate hind gut microbial community and metabolic markers in the pig. Plos ONE 8, e59581.CrossRefGoogle ScholarPubMed
Yang, YX, Mu, CL, Zhang, JF and Zhu, WY 2014. Determination of biogenic amines in digesta by high performance liquid chromatography with precolumn dansylation. Analytical Letters 47, 1290–1298.CrossRefGoogle Scholar
Yoon, JH, Ingale, SL, Kim, JS, Kim, KH, Lee, SH, Park, YK, Lee, SC, Kwon, IK and Chae, BJ 2014. Effects of dietary supplementation of synthetic antimicrobial peptide-A3 and P5 on growth performance, apparent total tract digestibility of nutrients, fecal and intestinal microflora and intestinal morphology in weanling pigs. Livestock Science 159, 53–60.CrossRefGoogle Scholar
Yu, M, Mu, C, Yang, Y, Zhang, C, Su, Y, Huang, Z, Yu, K and Zhu, W 2017. Increases in circulating amino acids with in-feed antibiotics correlated with gene expression of intestinal amino acid transporters in piglets. Amino Acids 49, 1587–1599.CrossRefGoogle ScholarPubMed
Zhang, C, Yu, M, Yang, Y, Mu, C, Su, Y and Zhu, W 2016a. Differential effect of early antibiotic intervention on bacterial fermentation patterns and mucosal gene expression in the colon of pigs under diets with different protein levels. Applied Microbiology and Biotechnology 101, 2493–2505.CrossRefGoogle ScholarPubMed
Zhang, C, Yu, M, Yang, Y, Mu, C, Su, Y and Zhu, W 2016b. Effect of early antibiotic administration on cecal bacterial communities and their metabolic profiles in pigs fed diets with different protein levels. Anaerobe 42, 188–196.CrossRefGoogle ScholarPubMed
Zoetendal, EG, Akkermans, AD and De Vos, WM 1998. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Applied and Environmental Microbiology 64, 3854–3859.CrossRefGoogle ScholarPubMed
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