The Effects of the antimicrobial peptide WK3 on diarrhea, growth performance and intestinal health of weaned piglets challenged with enterotoxigenic Escherichia coli K88

  • Licong Zhang Institute of Animal Nutrition, Northeast Agricultural University, Xiangfang District, Harbin, People’s Republic of China
  • Tao Guo Institute of Animal Nutrition, Northeast Agricultural University, Xiangfang District, Harbin, People’s Republic of China
  • Na Zhan Institute of Animal Nutrition, Northeast Agricultural University, Xiangfang District, Harbin, People’s Republic of China
  • Taotao Sun Institute of Animal Nutrition, Northeast Agricultural University, Xiangfang District, Harbin, People’s Republic of China
  • Anshan Shan Institute of Animal Nutrition, Northeast Agricultural University, Xiangfang District, Harbin, People’s Republic of China
Keywords: WK3, weaned piglets, diarrhea, growth performance, intestinal

Abstract

Background: Antibiotics are very effective for treating diarrhea in weaned pigs, but the global prohibition of antibiotics makes it urgent to find an alternative to antibiotics.

Objective: An experiment was conducted to determine the antimicrobial activity of a linear trpzip-like β-hairpin antimicrobial peptide WK3 in vivo and to assess its effects on growth performance and intestinal health.

Design: Thirty-two piglets were weaned at 21 days and housed in individual metabolic cages, which were randomly divided into four groups and were maintained on a corn-soybean meal-based basal diet. Group 1 included a blank group. Groups 2, 3, and 4 were orally infected by feeding with Enterotoxigenic Escherichia coli (ETEC) K88, which was followed by saline treatment (group 2), enrofloxacin injection at a dose of 2.5 mg/ kg (group 3), and WK3 injection at a dose of 2 mg/kg (group 4). The experiment lasted for 6 days, and feed and water were provided ad libitum.

Results: Both WK3 and enrofloxacin effectively attenuated diarrhea and improved growth performance of piglets. Compared with the control group, WK3 significantly improved the villus height in the ileum (P < 0.05) but did not affect the villus height in the duodenum or jejunum. Additionally, we did not observe any obvious difference in crypt depth or villus height/crypt depth among the duodenum, jejunum and ileum (P > 0.05). WK3 also reduced the numbers of Enterococcus spp (P < 0.01) in the cecal contents, and the number of Enterobacterium spp tended to decrease (0.05 < P < 0.1). Moreover, the jejunal mucosa of the WK3 group exhibited lower interleukin-1α (IL-1a; P < 0.01), toll-like receptors-4 (TLR-4; P < 0.05), and myeloid differentiation primary response 88 (MyD88; P < 0.01) messenger ribonucleic acid (mRNA) expression levels. The jejunum of the WK3 group also exhibited an increased antioxidant capacity, reduced concentration of malondialdehyde (MDA; P < 0.05), and enhanced superoxide dismutase (SOD) activity (P < 0.05).

Conclusions: WK3 has the potential to replace antibiotics as a new generation feed additive.

Downloads

Download data is not yet available.

References


  1. Rhouma M, Beaudry F, Theriault W, Bergeron N, Beauchamp G, Laurent-Lewandowski S, et al. In vivo therapeutic efficacy and pharmacokinetics of colistin sulfate in an experimental model of enterotoxigenic Escherichia coli infection in weaned pigs. Vet Res 2018; 47: 58. doi: 10.1186/s13567-016-0344-y

  2. Rhouma M, Fairbrother JM, Beaudry F, Letellier A. Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies. Acta Vet Scand 2017; 59: 31. doi: 10.1186/s13028-017-0299-7

  3. Li H, Zhang L, Chen L, Zhu Q, Wang W, Qiao J. Lactobacillus acidophilus alleviates the inflammatory response to enterotoxigenic Escherichia coli K88 via inhibition of the NF-κB and p38 mitogen-activated protein kinase signaling pathways in piglets. BMC Microbiol 2016; 16: 273. doi: 10.1186/s12866-016-0862-9

  4. Wang WW, Ma H, Yu HJ, Qin GY, Tan ZF, Wang YP, et al. Screening of Lactobacillus plantarum subsp. plantarum with potential probiotic activities for inhibiting ETEC k88 in weaned piglets. Molecules 2020; 25(19): e4481. doi: 10.3390/Molecules25194481

  5. Sen S, Ingale SL, Kim YW, Kim JS, Kim KH, Lohakare JD, et al. Effect of supplementation of Bacillus subtilis LS 1-2 to broiler diets on growth performance, nutrient retention, caecal microbiology and small intestinal morphology. Res Vet Sci 2012; 93: 264–8. doi: 10.1016/j.rvsc.2011.05.021

  6. Manafi M, Hedayati M, Pirany N, Omede AA. Comparison of performance and feed digestibility of the non-antibiotic feed supplement (NovacidTM) and an antibiotic growth promoter in broiler chickens. Poult Sci 2019; 98(6): 698. doi: 10.3382/ps/pey529

  7. Zhang L, Li G, Zhan N, Sun T, Cheng B, Li Y, et al. Expression of a Pseudomonas aeruginosa-targeted antimicrobial peptide T9W in Bacillus subtilis using a maltose-inducible vector. Process Biochem 2019; 81: 22–7. doi: 10.1016/j.procbio.2019.03.008

  8. Da CN, Cobacho NB, Viana JF, Lima LA, Sampaio KB, Dohms SS, et al. The next generation of antimicrobial peptides (AMPs) as molecular therapeutic tools for the treatment of diseases with social and economic impacts. Drug Discov Today 2017; 22: 234–48. doi: 10.1016/j.drudis.2016.10.017.

  9. Wang J, Dou X, Song J, Lyu Y, Zhu X, Xu L, et al. Antimicrobial peptides: promising alternatives in the post feeding antibiotic era. Med Res Rev 2019; 39(3): 831–59. doi: 10.1002/med.21542

  10. Xu L, Shao C, Li G, Shan A, Chou S, Wang J, et al. Conversion of broad-spectrum antimicrobial peptides into species-specific antimicrobials capable of precisely targeting pathogenic bacteria. Sci Rep 2020; 10(1): 994. doi: 10.1038/s41598-020-58014-6

  11. Liu YL, Ma AJ, Han PP, Chen Z, Jia YM. Antibacterial mechanism of brevilaterin B: an amphiphilic lipopeptide targeting the membrane of Listeria monocytogenes. Appl Microbiol Biot 2020; 104: 10531–39. doi: 10.1007/s00253-020-10993-2

  12. Wu S, Zhang F, Huang Z, Liu H, Xie C, Zhang J, et al. Effects of the antimicrobial peptide cecropin AD on performance and intestinal health in weaned piglets challenged with Escherichia coli. Peptides 2012; 35: 225–30. doi: 10.1016/j.peptides.2012.03.030

  13. Xu L, Chou S, Wang J, Shao C, Li W, Zhu X, et al. Antimicrobial activity and membrane-active mechanism of tryptophan zipper-like β-hairpin antimicrobial peptides. Amino Acids 2015; 47: 2385–97. doi: 10.1007/s00726-015-2029-7

  14. NRC. Nutrient requirements of swine. National Academies Press. Washington, DC;2012.

  15. Yu J, Song Y, Yu B, He J, Zheng P, Mao X, et al. Tannic acid prevents post-weaning diarrhea by improving intestinal barrier integrity and function in weaned piglets. Anim Reprod Sci 2020; 11: 87. doi: 10.1186/s40104-020-00496-5

  16. Yi H, Zhang L, Gan Z, Xiong H, Yu C, Du H, et al. High therapeutic efficacy of Cathelicidin-WA against postweaning diarrhea via inhibiting inflammation and enhancing epithelial barrier in the intestine. Sci Rep 2016; 6: 25679. doi: 10.1038/srep25679

  17. Yoon JH, Ingale SL, Kim JS, Kim KH, Lee SH, Park YK. Effects of dietary supplementation of antimicrobial peptide-A3 on growth performance, nutrient digestibility, intestinal and fecal microflora and intestinal morphology in weanling pigs. Anim Feed Sci Technol 2012; 177: 98–107. doi: 10.1016/j.anifeedsci.2012.06.009

  18. Xiong X, Yang H, Li L, Wang Y, Huang R, Li F, et al. Effects of antimicrobial peptides in nursery diets on growth performance of pigs reared on five different farms. Livest Sci 2014; 167: 206–10. doi: 10.1016/j.livsci.2014.04.024

  19. Feng J, Wang L, Xie Y, Chen Y, Yi H, He D. Effects of antimicrobial peptide cathelicidin-BF on diarrhea controlling, immune responses, intestinal inflammation and intestinal barrier function in piglets with postweaning diarrhea. Int Immunopharmacol 2020; 85: 106658. doi: 10.1016/j.intimp.2020.106658

  20. Wang JH, Wu CC, Feng J. Effect of dietary antibacterial peptide and zinc-methionine on performance and serum biochemical parameters in piglets. Czech J Anim Sci 2011; 56: 30–6. doi: 10.17221/341/2009-CJAS

  21. Yoon JH, Ingale SL, Kim JS, Kim KH, Lohakare J, Park YK, et al. Effects of dietary supplementation with antimicrobial peptide-P5 on growth performance, apparent total tract digestibility, faecal and intestinal microflora and intestinal morphology of weanling pigs. J Sci Food Agric 2013; 93: 587–92. doi: 10.1002/jsfa.5840

  22. Niu Y, He J, Zhao Y, Gan Z, Shen M, Zhang L, et al. Dietary enzymatically treated Artemisia annua L. supplementation improved growth performance and intestinal antioxidant capacity of weaned piglets. Livest Sci 2020; 232: 103937. doi: 10.1016/j.livsci.2020.103937

  23. Tang Z, Yin Y, Zhang Y, Huang R, Sun Z, Li T, et al. Effects of dietary supplementation with an expressed fusion peptide bovine lactoferricin-lactoferrampin on performance, immune function and intestinal mucosal morphology in piglets weaned at age 21 d. Br J Nutr 2009; 101: 998–1005. doi: 10.1017/S0007114508055633

  24. Jin Z, Yang YX, Choi JY, Shinde PL, Yoon SY, Hahn TW, et al. Effects of potato (Solanum tuberosum L. cv. Golden valley) protein having antimicrobial activity on the growth performance, and intestinal microflora and morphology in weanling pigs. Anim Feed Sci Technol 2008; 140: 139–54. doi: 10.1016/j.anifeedsci.2007.12.006

  25. Caspary WF. Physiology and pathophysiology of intestinal absorption. Am J Clin Nutr 1992; 55: 299S–308S. doi: 10.1093/ajcn/55.1.299s

  26. Fan YK, Croom J, Christensen VL, Black BL, Bird AR, Daniel LR, et al. Jejunal glucose uptake and oxygen consumption in turkey poults selected for rapid growth. Poult Sci 1997; 76: 1738. doi: 10.1093/ps/76.12.1738

  27. Wang R, Yu Hao, Fang H, Jin Y, Zhao Y, Shen J, et al. Effects of dietary grape pomace on the intestinal microbiota and growth performance of weaned piglets. Arch Anim Nutr 2020: 1–13. doi: 10.1080/1745039X.2020.1743607

  28. Mathew AG, Upchurch WG, Chattin SE. Incidence of antibiotic resistance in fecal Escherichia coli isolated from commercial swine farms. J Anim Sci 1998; 76: 429–34. doi: 10.2527/1998.762429x

  29. Brassart D, Schiffrin EJ. The use of probiotics to reinforce mucosal defence mechanisms. Trends Food Sci Technol 1997; 8: 321–6. doi: 10.1016/S0924-2244(97)01071-6

  30. Brown K, Decoffe D, Molcan E, Gibson DL. Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients 2012; 4: 1552–3. doi: 10.3390/nu4081095

  31. Suchodolski JS, Camacho J, Steiner JM. Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S r RNA gene analysis. FEMS Microbiol Ecol 2008; 66(3): 567–78. doi: 10.1111/j.1574-6941.2008.00521.x

  32. Wang J, Tian S, Yu H, Wang J, Zhu W. Response of colonic mucosa-associated microbiota composition, mucosal immune homeostasis, and barrier function to early life galactooligosaccharides intervention in suckling piglets. J Agric Food Chem 2019; 67: 578–88. doi: 10.1021/acs.jafc.8b05679

  33. Yi H, Yu C, Zhang H, Song D, Jiang D, Du H, et al. Cathelicidin-BF suppresses intestinal inflammation by inhibiting the nuclear factor-kappaB signaling pathway and enhancing the phagocytosis of immune cells via STAT-1 in weanling piglets. Int Immunopharmacol 2015; 28: 61–9. doi: 10.1016/j.intimp.2015.05.034

  34. Song D, Zong X, Zhang H, Wang T, Yi H, Luan C, et al. Antimicrobial peptide Cathelicidin-BF prevents intestinal barrier dysfunction in a mouse model of endotoxemia. Int Immunopharmacol 2015; 25: 141–7. doi: 10.1016/j.intimp.2015.01.017

  35. Wang J, Tian S, Wang J, Zhu W. Early galactooligosaccharide intervention alters the metabolic profile, improves the antioxidant capacity of mitochondria and activates the AMPK/Nrf2 signaling pathway in suckling piglet liver. Food Funct 2020; 11: 7280–92. doi: 10.1039/d0fo01486a

  36. Doyotte A, Cossu C, Jacquin MC, Babut M, Vasseur P. Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquat Toxicol 1997; 39: 93–110. doi: 10.1016/S0166-445X(97)00024-6

  37. Cheung CC, Zheng GJ, Li AM, Richardson BJ, Lam PK. Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis. Aquat Toxicol 2001; 52: 189. doi: 10.1016/S0166-445X(00)00145-4

  38. Wei B, Nie S, Meng Q, Qu Z, Shan A, Chen Z. Effects of L-carnitine and/or maize distillers dried grains with solubles in diets of gestating and lactating sows on the intestinal barrier functions of their offspring. Br J Nutr 2016; 116: 459–69. doi: 10.1017/S0007114516001951

  39. Liu Y, Han J, Huang J, Wang X, Wang F, Wang J. Dietary L-arginine supplementation improves intestinal function in weaned pigs after an Escherichia coli lipopolysaccharide challenge. Asian Australas J Anim 2009; 22: 1667–75. doi: 10.5713/ajas.2009.90100

Published
2021-05-12
How to Cite
Zhang L., Guo T., Zhan N., Sun T., & Shan A. (2021). The Effects of the antimicrobial peptide WK3 on diarrhea, growth performance and intestinal health of weaned piglets challenged with enterotoxigenic <em>Escherichia coli</em&gt; K88. Food & Nutrition Research, 65. https://doi.org/10.29219/fnr.v65.3448
Section
Original Articles