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Inclusion of Lacticaseibacillus paracasei NSMJ15 in broiler diets induces changes in jejunal immune cell population and cecal microbiota

  • June Hyeok Yoon (Research Institute for Innovative Animal Science, Kyungpook National University) ;
  • Sang Seok Joo (Department of Animal Science, College of Natural Resources and Life Science, Pusan National University) ;
  • Su Hyun An (Research Institute for Innovative Animal Science, Kyungpook National University) ;
  • Byeong Cheol Ban (Department of Animal Science, College of Natural Resources and Life Science, Pusan National University) ;
  • Moongyeong Jung (Department of Animal Science, College of Natural Resources and Life Science, Pusan National University) ;
  • Woonhak Ji (Department of Animal Science, College of Natural Resources and Life Science, Pusan National University) ;
  • Ji Young Jung (Biological Resources Research Department, Nakdonggang National Institute of Biological Resources (NNIBR)) ;
  • Myunghoo Kim (Department of Animal Science, College of Natural Resources and Life Science, Pusan National University) ;
  • Changsu Kong (Research Institute for Innovative Animal Science, Kyungpook National University)
  • 투고 : 2024.03.15
  • 심사 : 2024.06.10
  • 발행 : 2024.12.01

초록

Objective: The objective was to investigate growth performance, antioxidant enzyme activity, intestinal morphology, immune cell distribution, short chain fatty acid (SCFA) profile, and microbiota in broiler chickens fed a diet containing Lacticaseibacillus paracasei NSMJ15. Methods: A total of 120 1-day-old Ross 308 male broilers were allocated to 2 dietary treatments in a randomized complete block design. A control group was fed a corn-soybean meal control diet, and an NSMJ15-supplemented group was fed a control diet supplemented with 1 g/kg L. paracasei NSMJ15 at the expense of cornstarch. Each dietary treatment had 6 replicates with 10 birds per cage. Growth performance was recorded on day 9. On day 10, one bird representing median body weight was selected to collect serum for antioxidant enzyme activity, jejunal tissue for immune cell isolation and morphometric analysis, and cecal digesta for 16S rRNA gene sequencing and SCFA analysis. Results: Supplementation of L. paracasei NSMJ15 did not affect growth performance, serum antioxidant enzyme activity, and jejunal histomorphology compared to the control group. In the NSMJ15-supplemented group, the population of CD3+CD4+CD8- T cells increased (p = 0.010), while the population of CD3+CD8+TCRγδ+ T cells decreased (p = 0.022) compared to the control group. The L. paracasei NSMJ15 supplementation decreased (p = 0.022) acetate concentration in the cecal digesta compared to the control group. The 16S rRNA gene sequencing analysis showed that NSMJ15-supplemented group differentially expressed (p<0.05) 10 more amplicon sequence variants compared to control group without affecting alpha and beta diversity indices of the cecal microbiota. Genera Mediterraneibacter and Negativibacillus were positively (p<0.05) correlated with CD4+ T cells, while genera Gemmiger, Coprococcus, Sellimonas, Massilimicrobiota, and Blautia were negatively (p<0.05) correlated with SCFA concentration. Conclusion: The results of the present study suggest dietary L. paracasei NSMJ15 supplementation may increase percentage of CD4+ T cells and decrease acetate concentration in broiler chickens by increasing the differential expression of specific microbial genera.

키워드

과제정보

This work was supported by a Nakdonggang National Institute of Biological Resources grant (project no. NNIBR20243101) funded by the Ministry of Environment, Republic of Korea.

참고문헌

  1. Zhao L, Dong YH, Wang H. Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 2010;408:1069-75. https://doi.org/10.1016/j.scitotenv.2009.11.014 
  2. Xu Y, Yu Y, Shen Y, et al. Effects of Bacillus subtilis and Bacillus licheniformis on growth performance, immunity, short chain fatty acid production, antioxidant capacity, and cecal microflora in broilers. Poult Sci 2021;100:101358. https://doi.org/10.1016/j.psj.2021.101358 
  3. Mehdi Y, Letourneau-Montminy MP, Gaucher ML, et al. Use of antibiotics in broiler production: global impacts and alternatives. Anim Nutr 2018;4:170-8. https://doi.org/10.1016/j.aninu.2018.03.002 
  4. Blajman JE, Frizzo LS, Zbrun MV, et al. Probiotics and broiler growth performance: a meta-analysis of randomised controlled trials. Br Poult Sci 2014;55:483-94. https://doi.org/10.1080/00071668.2014.931930 
  5. Rajput IR, Li LY, Xin X, et al. Effect of Saccharomyces boulardii and Bacillus subtilis B10 on intestinal ultrastructure modulation and mucosal immunity development mechanism in broiler chickens. Poult Sci 2013;92:956-65. https://doi.org/10.3382/ps.2012-02845 
  6. Ma T, Suzuki Y, Guan LL. Dissect the mode of action of probiotics in affecting host-microbial interactions and immunity in food producing animals. Vet Immunol Immunopathol 2018;205:35-48. https://doi.org/10.1016/j.vetimm.2018.10.004 
  7. Jung JY, Han SS, Kim ZH, et al. In-vitro characterization of growth inhibition against the gut pathogen of potentially probiotic lactic acid bacteria strains isolated from fermented products. Microorganisms 2021;9:2141. https://doi.org/10.3390/microorganisms9102141 
  8. Aviagen. Ross 308 broiler: nutrition specification [Internet]. Newbridge, UK: Newbridge Aviagen Ltd; c2022 [cited 2024 Feb 14]. Available from: https://aviagen.com/assets/Tech_Center/Ross_Broiler/Ross-BroilerNutritionSpecifications2022-EN.pdf 
  9. Zhao Y, Zeng D, Wang H, et al. Dietary probiotic Bacillus licheniformis H2 enhanced growth performance, morphology of small intestine and liver, and antioxidant capacity of broiler chickens against Clostridium perfringens-induced subclinical necrotic enteritis. Probiotics Antimicrob Proteins 2020;12:883-95. https://doi.org/10.1007/s12602-019-09597-8 
  10. Sokale AO, Menconi A, Mathis GF, et al. Effect of Bacillus subtilis DSM 32315 on the intestinal structural integrity and growth performance of broiler chickens under necrotic enteritis challenge. Poult Sci 2019;98:5392-400. https://doi.org/10.3382/ps/pez368 
  11. Liu H, Ji HF, Zhang DY, et al. Effects of Lactobacillus brevis preparation on growth performance, fecal microflora and serum profile in weaned pigs. Livest Sci 2015;178:251-4. https://doi.org/10.1016/j.livsci.2015.06.002 
  12. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: a systematic review. Animals 2020;10:1863. https://doi.org/10.3390/ani10101863 
  13. Xu Y, Tian Y, Cao Y, et al. Probiotic properties of Lactobacillus paracasei subsp. paracasei L1 and its growth performance-promotion in chicken by improving the intestinal microflora. Front Physiol 2019;10:937. https://doi.org/10.3389/fphys.2019.00937 
  14. Gyawali I, Zeng Y, Zhou J, et al. Effect of novel Lactobacillus paracaesi microcapsule on growth performance, gut health and microbiome community of broiler chickens. Poult Sci 2022;101:101912. https://doi.org/10.1016/j.psj.2022.101912 
  15. Dowarah R, Verma AK, Agarwal N, Singh P, Singh BR. Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets. PLoS ONE 2018;13:e0192978. https://doi.org/10.1371/journal.pone.0192978 
  16. Reiner SL. Development in motion: helper T cells at work. Cell 2007;129:33-6. https://doi.org/10.1016/j.cell.2007.03.019 
  17. Wang L, Liu C, Chen M, et al. A novel Lactobacillus plantarum strain P-8 activates beneficial immune response of broiler chickens. Int Immunopharmacol 2015;29:901-7. https://doi.org/10.1016/j.intimp.2015.07.024 
  18. Meyer MM, Fries-Craft KA, Bobeck EA. Composition and inclusion of probiotics in broiler diets alter intestinal permeability and spleen immune cell profiles without negatively affecting performance. J Anim Sci 2020;98:skz383. https://doi.org/10.1093/jas/skz383 
  19. van der Hee B, Wells JM. Microbial regulation of host physiology by short-chain fatty acids. Trends Microbiol 2021;29:700-12. https://doi.org/10.1016/j.tim.2021.02.001 
  20. Shang Y, Kumar S, Oakley B, Kim WK. Chicken gut microbiota: importance and detection technology. Front Vet Sci 2018;5:254. https://doi.org/10.3389/fvets.2018.00254 
  21. Choi KY, Lee TK, Sul WJ. Metagenomic analysis of chicken gut microbiota for improving metabolism and health of chickens - a review. Asian-Australas J Anim Sci 2015;28:1217-25. https://doi.org/10.5713/ajas.15.0026 
  22. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006;444:1022-3. https://doi.org/10.1038/4441022a 
  23. Huang Y, Lv H, Song Y, Sun C, Zhang Z, Chen S. Community composition of cecal microbiota in commercial yellow broilers with high and low feed efficiencies. Poult Sci 2021;100:100996. https://doi.org/10.1016/j.psj.2021.01.019 
  24. Farkas V, Csitari G, Menyhart L, et al. Microbiota composition of mucosa and interactions between the microbes of the different gut segments could be a factor to modulate the growth rate of broiler chickens. Animals 2022;12:1296. https://doi.org/10.3390/ani12101296 
  25. Liu J, Robinson K, Lyu W, et al. Anaerobutyricum and subdoligranulum are differentially enriched in broilers with disparate weight gains. Animals 2023;13:1834. https://doi.org/10.3390/ani13111834 
  26. Lourenco JM, Nunn SC, Lee EJ, Dove CR, Callaway TR, Azain MJ. Effect of supplemental protease on growth performance and excreta microbiome of broiler chicks. Microorganisms 2020;8:475. https://doi.org/10.3390/microorganisms8040475 
  27. Zhou Q, Lan F, Li X, et al. The spatial and temporal characterization of gut microbiota in broilers. Front Vet Sci 2021;8:712226. https://doi.org/10.3389/fvets.2021.712226 
  28. Song J, Li Q, Everaert N, et al. Dietary inulin supplementation modulates short-chain fatty acid levels and cecum microbiota composition and function in chickens infected with salmonella. Front Microbiol 2020;11:584380. https://doi.org/10.3389/fmicb.2020.584380 
  29. Yang S, Yang Y, Long X, Li H, Zhang F, Wang Z. Integrated analysis of the effects of cecal microbiota and serum metabolome on market weights of Chinese native chickens. Animals 2023;13:3034. https://doi.org/10.3390/ani13193034 
  30. Liu L, Lin L, Zheng L, et al. Cecal microbiome profile altered by Salmonella enterica, serovar Enteritidis inoculation in chicken. Gut Pathog 2018;10:34. https://doi.org/10.1186/s13099-018-0261-x 
  31. Kong L, Wang Z, Xiao C, Zhu Q, Song Z. Glycerol monolaurate attenuated immunological stress and intestinal mucosal injury by regulating the gut microbiota and activating AMPK/Nrf2 signaling pathway in lipopolysaccharide-challenged broilers. Anim Nutr 2022;10:347-59. https://doi.org/10.1016/j.aninu.2022.06.005 
  32. Zhou Y, Zhang M, Liu Q, Feng J. The alterations of tracheal microbiota and inflammation caused by different levels of ammonia exposure in broiler chickens. Poult Sci 2021;100:685-96. https://doi.org/10.1016/j.psj.2020.11.026 
  33. Caudill MT, Brayton KA. The use and limitations of the 16S rRNA sequence for species classification of anaplasma samples. Microorganisms 2022;10:605. https://doi.org/10.3390/microorganisms10030605