Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Bacillus subtilis improves antioxidant capacity and optimizes inflammatory state in broilers

  • Yu Zhang (Animal Science and Technology College, Beijing University of Agriculture) ;
  • Junyan Zhou (Animal Science and Technology College, Beijing University of Agriculture) ;
  • Linbao Ji (College of Animal Science and Technology, China Agricultural University) ;
  • Lian Zhang (College of Animal Science and Technology, China Agricultural University) ;
  • Liying Zhao (Animal Science and Technology College, Beijing University of Agriculture) ;
  • Yubing Guo (Animal Science and Technology College, Beijing University of Agriculture) ;
  • Haitao Wei (Animal Science and Technology College, Beijing University of Agriculture) ;
  • Lin Lu (Animal Science and Technology College, Beijing University of Agriculture)
  • Received : 2023.08.27
  • Accepted : 2024.01.08
  • Published : 2024.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Bacillus subtilis, a kind of probiotic with broad-spectrum antibacterial function, was commonly used in livestock and poultry production. Recent research suggested that Bacillus subtilis may have antioxidant properties and improve immune response. This study aimed to verify the probiotic function of Bacillus subtilis in the production of broiler chickens. Methods: A total of 324 (1-day-old) Arbor Acres broilers were selected and randomly divided into three groups: basal diet group (Ctr Group), basal diet + antibiotic growth promoter group (Ctr + AGP) and basal diet + 0.5% Bacillus subtilis preparation group (Ctr + Bac). The experiment lasted for 42 days. Muscle, serum and liver samples were collected at 42 days for determination. Results: The results showed that Bacillus subtilis could decrease malondialdehyde content in the serum and liver (p<0.05) and increase superoxide dismutase 1 mRNA expression (p<0.01) and total superoxide dismutase (p<0.05) in the liver. In addition, compared with AGP supplementation, Bacillus subtilis supplementation increased interleukin-10 (IL-10) and decreased tumor necrosis factor-α and IL-1β level in the serum (p<0.05). At 45 minutes after slaughter Ctr + Bac presented a higher a* value of breast muscle than Ctr Group (p<0.05), while significant change in leg muscle was not identified. Moreover, there was no difference in weight, shear force, cooking loss and drip loss of breast and leg muscle between treatments. Conclusion: Our results demonstrate that Bacillus subtilis in diet can enhance antioxidant capacity and optimize immune response of broilers.

Keywords

Acknowledgement

This work was financially supported by the Beijing Innovation Team of the Modern Agricultural Research System BAIC08-2024-SYZ03 and Science and Technology innovation support program of Beijing University of Agriculture (BUA-HHXD2023009).

References

  1. Jiang H, Zhang XW, Liao QL, Wu WT, Liu YL, Huang WH. Electrochemical monitoring of paclitaxel-induced ROS release from mitochondria inside single cells. Small 2019;15:1901787. https://doi.org/10.1002/smll.201901787
  2. Kim HO, Yeom MJ, Kim JH, et al. Reactive oxygen species-regulating polymersome as an antiviral agent against influenza virus. Small 2017;13:1700818. https://doi.org/10.1002/smll.201700818
  3. Schurmann N, Forrer P, Casse O, et al. Myeloperoxidase targets oxidative host attacks to Salmonella and prevents collateral tissue damage. Nat Microbiol 2017;2:16268. https://doi.org/10.1038/nmicrobiol.2016.268
  4. Henry C, Loiseau L, Vergnes A, et al. Redox controls RecA protein activity via reversible oxidation of its methionine residues. eLife 2021;10:e63747. https://doi.org/10.7554/eLife.63747
  5. Diwanji N, Bergmann A. Basement membrane damage by ROS- and JNK-mediated Mmp2 activation drives macrophage recruitment to overgrown tissue. Nat Commun 2020;11:3631. https://doi.org/10.1038/s41467-020-17399-8
  6. Hunyadi A. The mechanism(s) of action of antioxidants: from scavenging reactive oxygen/nitrogen species to redox signaling and the generation of bioactive secondary metabolites. Med Res Rev 2019;39:2505-33. https://doi.org/10.1002/med.21592
  7. Cafe SL, Nixon B, Dun MD, Roman SD, Bernstein IR, Bromfield EG. Oxidative stress dysregulates protein homeostasis within the male germ line. Antioxid Redox Signal 2020;32:487-503. https://doi.org/10.1089/ars.2019.7832
  8. Chen Z, Wang C, Yu N, et al. INF2 regulates oxidative stress-induced apoptosis in epidermal HaCaT cells by modulating the HIF1 signaling pathway. Biomed Pharmacother 2019;111:151-61. https://doi.org/10.1016/j.biopha.2018.12.046
  9. Dikalov SI, Dikalova AE. Crosstalk between mitochondrial hyperacetylation and oxidative stress in vascular dysfunction and hypertension. Antioxid Redox Signal 2019;31:710-21. https://doi.org/10.1089/ars.2018.7632
  10. Kotani K, Watanabe J, Miura K, Gugliucci A. Paraoxonase 1 and non-alcoholic fatty liver disease: a meta-analysis. Molecules 2021;26:2323. https://doi.org/10.3390/molecules26082323
  11. Di Stefano A, Maniscalco M, Balbi B, Ricciardolo FLM. Oxidative and nitrosative stress in the pathogenesis of obstructive lung diseases of increasing severity. Curr Med Chem 2020;27:7149-58. https://doi.org/10.2174/0929867327666200604165451
  12. Chen GY, Nunez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 2010;10:826-37. https://doi.org/10.1038/nri2873
  13. Saunders LP, Bischoff KM, Bowman MJ, Leathers TD. Inhibition of Lactobacillus biofilm growth in fuel ethanol fermentations by Bacillus. Bioresour Technol 2019;272:156-61. https://doi.org/10.1016/j.biortech.2018.10.016
  14. Li J, Islam S, Guo P, Hu X, Dong W. Isolation of antimicrobial genes from Oryza rufipogon griff by using a Bacillus subtilis expression system with potential antimicrobial activities. Int J Mol Sci 2020;21:8722. https://doi.org/10.3390/ijms21228722
  15. Huang B, Wang J, Han X, et al. The relationship between material transformation, microbial community and amino acids and alkaloid metabolites in the mushroom residue-prickly ash seed oil meal composting with biocontrol agent addition. Bioresour Technol 2022;350:126913. https://doi.org/10.1016/j.biortech.2022.126913
  16. Ruan S, Li Y, Wang Y, Huang S, Luo J, Ma H. Analysis in protein profile, antioxidant activity and structure-activity relationship based on ultrasound-assisted liquid-state fermentation of soybean meal with Bacillus subtilis. Ultrason Sonochem 2020;64:104846. https://doi.org/10.1016/j.ultsonch.2019.104846
  17. Cui J, Xia P, Zhang L, Hu Y, Xie Q, Xiang H. A novel fermented soybean, inoculated with selected Bacillus, Lactobacillus and Hansenula strains, showed strong antioxidant and anti-fatigue potential activity. Food Chem 2020;333:127527. https://doi.org/10.1016/j.foodchem.2020.127527
  18. Rahman MS, Choi YH, Choi YS, Alam MB, Lee SH, Yoo JC. A novel antioxidant peptide, purified from Bacillus amyloliquefaciens, showed strong antioxidant potential via Nrf-2 mediated heme oxygenase-1 expression. Food Chem 2018;239:502-10. https://doi.org/10.1016/j.foodchem.2017.06.106
  19. Fotina AA, Fisinin VI, Surai PF. Recent developments in usage of natural antioxidants to improve chicken meat production and quality. Bulg J Agric Sci 2013;19:889-96.
  20. Surai PF. The antioxidant properties of canthaxanthin and its potential effects in the poultry eggs and on embryonic development of the chick, Part 1. Worlds Poult Sci J 2012;68:465-76. https://doi.org/10.1017/S0043933912000578
  21. Xing JH, Zhao W, Li QY, et al. Bacillus subtilis BSH has a protective effect on Salmonella infection by regulating the intestinal flora structure in chickens. Microb Pathog 2021;155:104898. https://doi.org/10.1016/j.micpath.2021.104898
  22. Bai K, Huang Q, Zhang J, He J, Zhang L, Wang T. Supplemental effects of probiotic Bacillus subtilis fmbJ on growth performance, antioxidant capacity, and meat quality of broiler chickens. Poult Sci 2017;96:74-82. https://doi.org/10.3382/ps/pew246
  23. Singh Z, Karthigesu IP, Singh P, Kaur R. Use of malondialdehyde as a biomarker for assessing oxidative stress in different disease pathologies: a review. Iran J Public Health 2014;43:7-16.
  24. Zhang Y, Chen SY, Hsu T, Santella RM. Immunohistochemical detection of malondialdehyde-DNA adducts in human oral mucosa cells. Carcinogenesis 2002;23:207-11. https://doi.org/10.1093/carcin/23.1.207
  25. Fukai T, Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 2011;15:1583-606. https://doi.org/10.1089/ars.2011.3999
  26. Eleutherio ECA, Silva Magalhaes RS, de Araujo Brasil A, Monteiro Neto JR, de Holanda Paranhos L. SOD1, more than just an antioxidant. Arch Biochem Biophys 2021;697:108701. https://doi.org/10.1016/j.abb.2020.108701
  27. Zhao XJ, Yu HW, Yang YZ, et al. Polydatin prevents fructose-induced liver inflammation and lipid deposition through increasing miR-200a to regulate Keap1/Nrf2 pathway. Redox Biol 2018;18:124-37. https://doi.org/10.1016/j.redox.2018.07.002
  28. Leake I. Choline uptake is vital for IL-1β-driven inflammation. Nat Rev Rheumatol 2019;15:320. https://doi.org/10.1038/s41584-019-0228-4
  29. Sorokin AV, Mehta NN. The relationship between TNF-alpha driven inflammation, lipids, and endothelial function in rheumatoid arthritis: a complex puzzle continues. Cardiovasc Res 2022;118:10-2. https://doi.org/10.1093/cvr/cvab190
  30. Toita R, Kawano T, Murata M, Kang JH. Anti-obesity and anti-inflammatory effects of macrophage-targeted interleukin10-conjugated liposomes in obese mice. Biomaterials 2016;110:81-8. https://doi.org/10.1016/j.biomaterials.2016.09.018
  31. Geginat J, Larghi P, Paroni M, et al. The light and the dark sides of Interleukin-10 in immune-mediated diseases and cancer. Cytokine Growth Factor Rev 2016;30:87-93. https://doi.org/10.1016/j.cytogfr.2016.02.003
  32. Saxton RA, Tsutsumi N, Su LL, et al. Structure-based decoupling of the pro- and anti-inflammatory functions of interleukin10. Science 2021;371:eabc8433. https://doi.org/10.1126/science.abc8433
  33. Coleman LG Jr, Zou J, Qin L, Crews FT. HMGB1/IL-1β complexes regulate neuroimmune responses in alcoholism. Brain Behav Immun 2018;72:61-77. https://doi.org/10.1016/j.bbi.2017.10.027
  34. Ye LL, Wei XS, Zhang M, Niu YR, Zhou Q. The significance of tumor necrosis factor receptor Type II in CD8+regulatory T cells and CD8+effector T cells. Front Immunol 2018;9:583. https://doi.org/10.3389/fimmu.2018.00583
  35. Salomon BL, Leclerc M, Tosello J, Ronin E, Piaggio E, Cohen JL. Tumor necrosis factor α and regulatory T cells in oncoimmunology. Front Immunol 2018;9:444. https://doi.org/10.3389/fimmu.2018.00444
  36. Chen X, Zhao H, Lu Y, Meng F, Lu Z, Lu Y. Surfactin mitigates dextran sodium sulfate-induced colitis and behavioral disorders in mice by mediating gut-brain-axis balance. J Agric Food Chem 2023;71:1577-92. https://doi.org/10.1021/acs.jafc.2c07369
  37. Zhao H, Shao D, Jiang C, et al. Biological activity of lipopeptides from Bacillus. Appl Microbiol Biotechnol 2017;101:5951-60. https://doi.org/10.1007/s00253-017-8396-0
  38. Mir NA, Rafiq A, Kumar F, Singh V, Shukla V. Determinants of broiler chicken meat quality and factors affecting them: a review. J Food Sci Technol 2017;54:2997-3009. https://doi.org/10.1007/s13197-017-2789-z
  39. Wang X, Wang Z, Zhuang H, et al. Changes in color, myoglobin, and lipid oxidation in beef patties treated by dielectric barrier discharge cold plasma during storage. Meat Sci 2021;176:108456. https://doi.org/10.1016/j.meatsci.2021.108456
  40. Sato H, Hayashi T, Ando T, Hisaeda Y, Ueno T, Watanabe Y. Hybridization of modified-heme reconstitution and distal histidine mutation to functionalize sperm whale myoglobin. J Am Chem Soc 2004;126:436-7. https://doi.org/10.1021/ja038798k
  41. Wang Z, Tu J, Zhou H, Lu A, Xu B. A comprehensive insight into the effects of microbial spoilage, myoglobin autoxidation, lipid oxidation, and protein oxidation on the discoloration of rabbit meat during retail display. Meat Sci 2021;172:108359. https://doi.org/10.1016/j.meatsci.2020.108359
  42. Wilson SA, Kroll T, Decreau RA, et al. Iron L-edge X-ray absorption spectroscopy of oxy-picket fence porphyrin: experimental insight into Fe-O2 bonding. J Am Chem Soc 2013;135:1124-36. https://doi.org/10.1021/ja3103583
  43. Bak KH, Bolumar T, Karlsson AH, Lindahl G, Orlien V. Effect of high pressure treatment on the color of fresh and processed meats: a review. Crit Rev Food Sci Nutr 2019;59:228-52. https://doi.org/10.1080/10408398.2017.1363712
  44. Wei Y, Li C, Zhang L, Su Z, Xu X. Inhibition of methemoglobin formation in aqueous solutions under aerobic conditions by the addition of amino acids. Int J Biol Macromol 2014;64:267-75. https://doi.org/10.1016/j.ijbiomac.2013.12.010
  45. Kumar Y, Yadav DN, Ahmad T, Narsaiah K. recent trends in the use of natural antioxidants for meat and meat products. Compr Rev Food Sci Food Saf 2015;14:796-812. https://doi.org/10.1111/1541-4337.12156
  46. Karre L, Lopez K, Getty KJK. Natural antioxidants in meat and poultry products. Meat Sci 2013;94:220-7. https://doi.org/10.1016/j.meatsci.2013.01.007