Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-25T22:35:15.734Z Has data issue: false hasContentIssue false
  • English
  • Français

Protein restriction and succedent realimentation affecting ileal morphology, ileal microbial composition and metabolites in weaned piglets

Published online by Cambridge University Press:  14 May 2019

Q. Shi ,
Y. Zhu ,
J. Wang ,
H. Yang ,
J. Wang Open the ORCID record for J. Wang [Opens in a new window]  and
W. Zhu
Q. Shi
Affiliation:
National center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
Y. Zhu
Affiliation:
National center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
J. Wang*
Affiliation:
National center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
H. Yang
Affiliation:
National center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
J. Wang*
Affiliation:
National center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
W. Zhu
Affiliation:
National center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
*
†E-mail: [email protected]
†E-mail: [email protected]
Get access

Abstract

Dietary protein restriction is one of the effective ways to reduce post-weaning diarrhoea and intestinal fermentation in piglets, but it may also reduce growth performance. The compensatory growth induced by subsequent protein realimentation may solve the issue. However, little research has been done on the impact of protein realimentation on the gut. In this study, the effects of protein restriction and realimentation on ileal morphology, ileal microbial composition and metabolites in weaned piglets were investigated. Thirty-six 28-day-old weaned piglets with an average body weight of 6.47 ± 0.04 kg were randomly divided into a control group and a treatment group. The CP level in the diet of the control group was 18.83% for the entire experimental period. The piglets in the treatment group were fed 13.05% CP between days 0 and 14 and restored to a diet of 18.83% CP for days 14 to 28. On day 14 and 28, six pigs from each group were sacrificed and sampled. It was found that the abundance of Lactobacillus and Salmonella in the ileal digesta was significantly lower in the treatment group than the control group on day 14, whereas the abundance of Clostridium sensu stricto 1, Streptococcus, Halomonas and Pseudomonas significantly increased in the ileal digesta of the treatment group on day 14 compared with the control group. In addition, reduced concentrations of lactic acid, total short-chain fatty acids (total SCFAs), total branched chain fatty acids, ammonia and impaired ileal morphology and mucosal barrier were observed in the treatment group on day 14. However, diarrhoea levels decreased in the treatment group throughout the experiment. During the succedent protein realimentation stage, the treatment group demonstrated compensatory growth. Compared with the control group, the treatment group showed increased abundance of Lactobacillus and reduced abundance of Salmonella, Halomonas and Pseudomonas in the ileum on day 28. The concentrations of lactic acid and total SCFAs increased significantly, whereas the concentration of ammonia remained at a lower level in the treatment group on day 28 compared with the control group. Overall, protein realimentation could improve ileal morphology and barrier functions and promote ileal digestive and absorptive functions. In conclusion, ileal microbial composition and metabolites could change according to dietary protein restriction and realimentation and eventually influence ileal morphology and barrier functions.

Keywords

pigslow proteincompensatory growthdiarrhoeaileal microbiota
Type
Research Article
Information
animal , Volume 13 , Issue 11 , November 2019 , pp. 2463 - 2472
Copyright
© The Animal Consortium 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Present address: Laboratory of Gastrointestinal Microbiology, Xiaolingwei Street, Weigang 1, Nanjing, China.

References

Aumiller, T, Mosenthin, R and Weiss, E 2014. Potential of cereal grains and grain legumes in modulating pig’s intestinal microbiota-A review. Livestock Science 172, 16–32.CrossRefGoogle Scholar
Caporaso, JG, Lauber, CL, Walters, WA, Berg-Lyons, D, Huntley, J, Fierer, N, Owens, SM, Betley, J, Fraser, L, Bauer, M, Gormley, N, Gilbert, JA, Smith, G and Knight, R 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6, 1621–1624.CrossRefGoogle ScholarPubMed
Chaosap, C, Parr, T, Wiseman, J 2011. Effect of compensatory growth on performance, carcass composition and plasma IGF-1 in grower finisher pigs. Animal 5, 749–756.CrossRefGoogle ScholarPubMed
Chasiotis, H, Kolosov, D, Bui, P and Kelly, SP 2012. Tight junctions, tight junction proteins and paracellular permeability across the gill epithelium of fishes: a review. Respiratory Physiology and Neurobiology 184, 269–281.CrossRefGoogle Scholar
Diao, H, Jiao, AR, Yu, B, He, J, Yu, J, Zheng, P, Huang, ZQ, Luo, YH, Luo, JQ, Mao, XB and Chen, DW 2017. Stimulation of intestinal growth with distal ileal infusion of short-chain fatty acid: a reevaluation in a pig model. RSC Advances 7, 30792–30806.CrossRefGoogle Scholar
Edgar, RC 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle ScholarPubMed
Eisenmenger, M 2009. Post weaning diarrhoea. In Paper Presented at the 25th Allen D. Lemon Swine Conference, 40–41 October 2009, Saint Paul, America.Google Scholar
Fan, P, Liu, P, Song, P, Chen, X and Ma, X 2017. Moderate dietary protein restriction alters the composition of gut microbiota and improves ileal barrier function in adult pig model. Scientific Reports 7, 43412.CrossRefGoogle ScholarPubMed
Gu, XH and Li, DF 2001. Dietary protein requirement and its effect on weaning pigs. China Agricultural Science and Technology 3, 34–37.Google Scholar
Hamer, HM, Jonkers, D, Venema, K, Vanhoutvin, S, Troost, FJ and Brummer, RJ 2008. Review article: the role of butyrate on colonic function. Alimentary Pharmacology and Therapeutics 27, 104–119.CrossRefGoogle ScholarPubMed
Heo, JM, Kim, JC, Yoo, J and Pluske, JR 2015. A between-experiment analysis of relationships linking dietary protein intake and post-weaning diarrhea in weanling piglets under conditions of experimental infection with an enterotoxigenic strain of Escherichia coli . Animal Science Journal 86, 286–293.CrossRefGoogle Scholar
Herfel, TM, Jacobi, SK, Lin, X, Fellner, V, Walker, DC, Jouni, ZE and Odle, J 2011. Polydextrose enrichment of infant formula demonstrates prebiotic characteristics by altering intestinal microbiota, organic acid concentrations, and cytokine expression in suckling piglets. Journal of Nutrition 141, 2139–2145.CrossRefGoogle ScholarPubMed
Hughes, R, Kurth, MJ, McGilligan, V, McGlynn, H and Rowland, I 2008. Effect of colonic bacterial metabolites on Caco-2 cell paracellular permeability in vitro. Nutrition and Cancer 60, 259–266.CrossRefGoogle ScholarPubMed
Ji, Y, Kong, X, Li, H, Zhu, Q, Guo, Q and Yin, Y 2017. Effects of dietary nutrient levels on microbial community composition and diversity in the ileal contents of pregnant Huanjiang mini-pigs. PloS ONE 12, e0172086.CrossRefGoogle ScholarPubMed
Madsen, JG, Bee, G 2015. Compensatory growth feeding strategy does not overcome negative effects on growth and carcass composition of low birth weight pigs. Animal 9, 427–436.CrossRefGoogle Scholar
Mao, S, Zhang, M, Liu, J and Zhu, W 2015. Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Scientific Reports 5, 16116.CrossRefGoogle ScholarPubMed
McLamb, BL, Gibson, AJ, Overman, EL, Stahl, C and Moeser, AJ 2013. Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli challenge and exacerbates intestinal injury and clinical disease. PloS ONE 8, e59838.CrossRefGoogle ScholarPubMed
Nyachoti, CM, Omogbenigun, FO, Rademacher, M and Blank, G 2006. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. Journal of Animal Science 84, 125–134.CrossRefGoogle ScholarPubMed
Palleroni, NJ 1981. Introduction to the family Pseudomonadaceae. In The Prokaryotes (eds Starr, MP, Stolp, H, Trüper, HG, Balows, A and Schlegel, HG), pp. 655–665. Springer, Berlin, Heidelberg.CrossRefGoogle Scholar
Piccolo, BD, Mercer, KE, Bhattacharyya, S, Bowlin, AK, Saraf, MK, Pack, L, Chintapalli, SV, Shankar, K, Adams, SH, Badger, TM and Yeruva, L 2017. Early postnatal diets affect the bioregional small intestine microbiome and ileal metabolome in neonatal pigs. The Journal of Nutrition 147, 1499–1509.CrossRefGoogle ScholarPubMed
Pieper, R, Tudela, CV, Taciak, M, Bindelle, J, Pérez, JF and Zentek, J 2016. Health relevance of intestinal protein fermentation in young pigs. Animal Health Research Reviews 17, 137–147.CrossRefGoogle ScholarPubMed
Pond, WG, Ellis, KJ, Mersmann, HJ, Heath, JP, Krook, LP, Burrin, DG, Dudley, MA and Sheng, HP 1996. Severe protein deficiency and repletion alter body and brain composition and organ weights in infant pigs. Journal of Nutrition 126, 290–302.CrossRefGoogle ScholarPubMed
Shi, C, Zhu, Y, Niu, Q, Wang, J, Wang, J and Zhu, W 2018. The changes of colonic bacterial composition and bacterial metabolism induced by an early food introduction in a neonatal porcine model. Current Microbiology 75, 745–751.CrossRefGoogle Scholar
Stein, HH and Kil, DY 2006. Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, part 2. Animal Biotechnology 17, 217–231.CrossRefGoogle ScholarPubMed
Sugiharto, S, Poulsen, A-SR, Canibe, N and Lauridsen, C 2015. Effect of bovine colostrum feeding in comparison with milk replacer and natural feeding on the immune responses and colonisation of enterotoxigenic Escherichia coli in the intestinal tissue of piglets. British Journal of Nutrition 113, 923–934.CrossRefGoogle ScholarPubMed
Tossou, MC, Liu, H, Bai, M, Chen, S, Cai, Y, Duraipandiyan, V, Liu, H, Adebowale, TO, Aldhabi, NA, Long, L 2016. Effect of high dietary tryptophan on intestinal morphology and tight junction protein of weaned pig. Biomed Research International 2, 1–6.CrossRefGoogle Scholar
Villodre Tudela, C, Boudry, C, Stumpff, F, Aschenback, JR, Vahjen, W, Zentek, J and Pieper, R 2015. Down-regulation of monocarboxylate transporter 1 (MCT1) gene expression in the colon of piglets is linked to bacterial protein fermentation and pro-inflammatory cytokine-mediated signalling. British Journal of Nutrition 113, 610–617.CrossRefGoogle Scholar
Vijayaraghavan, P and Vincent, SGP 2012. Cow dung as a novel, inexpensive substrate for the production of a halo-tolerant alkaline protease by Halomonas sp. PV1 for eco-friendly applications. Biochemical Engineering Journal 69, 57–60.CrossRefGoogle Scholar
Yue, LY and Qiao, SY 2008. Effects of low-protein diets supplemented with crystalline amino acids on performance and intestinal development in piglets over the first 2 weeks after weaning. Livestock Science 115, 144–152.CrossRefGoogle Scholar
Zhou, LZ, Fang, LD, Sun, Y, Su, Y and Zhu, WY 2016. Effects of the dietary protein level on the microbial compositon and metabolomic profile in the hindgut of the pig. Anaerobe 38, 61–69.CrossRefGoogle Scholar
Zhou, XL, Kong, XF, Yang, XJ and Yin, YL 2012. Soybean oligosaccharides alter colon short-chain fatty acid production and microbial population in vitro. Journal of Animal Science 90, 37–39.CrossRefGoogle ScholarPubMed
Zhu, Y, Niu, Q, Shi, C, Wang, J and Zhu, W 2017. The role of microbiota in compensatory growth of protein-restricted rats. Microbial Biotechnology 10, 480–491.CrossRefGoogle ScholarPubMed
Zhu, Y, Shi, C, Niu, Q, Wang, J and Zhu, W 2018. Dynamic changes in morphology, gene expression and microbiome in the jejunum of compensatory-growth rats induced by protein restriction. Microbial Biotechnology 11, 734–746.CrossRefGoogle ScholarPubMed
Zoetendal, EG, Akkermans, ADL and Vos, WMD 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.Google ScholarPubMed
Supplementary material: File

Shi et al. supplementary material

Shi et al. supplementary material 1

Download Shi et al. supplementary material(File)
File 399.3 KB