Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Effects of Lactococcus lactis subsp. lactis I2 with β-Glucooligosaccharides on Growth, Innate Immunity and Streptococcosis Resistance in Olive Flounder (Paralichthys olivaceus)

  • Received : 2018.05.11
  • Accepted : 2018.08.03
  • Published : 2018.09.28
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Abstract

To identify and quantify the effects of a combination of dietary $1{\times}10^8CFU/g$ Lactococcus lactis subsp. lactis I2 ($LI_2$) and 0.1% ${\beta}$-glucooligosaccharides (BGO) on the growth and immunity of olive flounder (Paralichthys olivaceus), a feeding experiment was conducted. Flounder ($14{\pm}0.5g$) were divided into two groups and fed control and synbiotic feeds for 8 weeks. Investigations were carried out on growth and feed utilization, innate immunity, serum biochemical parameters, intestinal lactic acid bacterial (LAB) viability, microvillus length, and changes in the expression levels of genes encoding pro-inflammatory cytokines (tumor necrosis factor $[TNF]-{\alpha}$, interleukin $[IL]-1{\beta}$, and IL-6). Results demonstrated the synbiotic diet had significantly better (p < 0.05) responses in terms of weight gain and specific growth rate, three innate immune parameters (respiratory burst, serum lysozyme, and superoxide dismutase), intestinal LAB viability, and the relative $TNF-{\alpha}$ expression level (p < 0.05). Moreover, after challenge with Streptococcus iniae ($1{\times}10^8CFU/ml$), the synbiotically fed group exhibited significantly higher (p < 0.05) protection against streptococcosis, validating the observed changes in immune parameters and induction of the cytokine-encoding gene. Therefore, according to the results of the present study, synbiotic feed ($LI_2+BGO$) increased growth, modulated innate immune parameters and protected olive flounder against streptococcosis.

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References

  1. Statistics Korea (KOSTAT): Republic of Korea: 2016 Survey on the status of fish culture (Proposed). Available from http://kostat.go.kr/portal/korea/kor_nw/2/7/1/index.board?bmode=read&aSeq=359717
  2. Norwood C. (World Aquaculture Society's 2015 annual conference) Flatfish spearhead South Korea' saquaculture exports. FISH 23: 28-29. Available from http://www.frdc.com.au/knowledge/publications/fish/Pages/23-3_articles/28-Flatfish-spearhead.aspx#sthash.MRckN1r1.dpuf
  3. Heo WS, Kim YR, Kim EY, Bai SC, Kong IS. 2013. Effects of dietary probiotic, Lactococcus lactis subsp. lactis I2, supplementation on the growth and immune response of olive flounder (Paralichthys olivaceus). Aquaculture 376: 20-24.
  4. Park YK, Nho SW, Shin GW, Park SB, Jang HB, Cha IS, et al. 2009. Antibiotic susceptibility and resistance of Streptococcus iniae and Streptococcus parauberis isolated from olive flounder (Paralichthys olivaceus). Vet. Microbiol. 136: 76-81. https://doi.org/10.1016/j.vetmic.2008.10.002
  5. World Health Organization (WHO). 2006 Report of a joint FAO/OIE/WHO expert consultation on antimicrobial use in aquaculture and antimicrobial resistance. Seoul, Republic of Korea, 13-16 June, 2006.
  6. Kwon SR, Lee EH, Nam YK, Kim SK, Kim KH. 2007. Efficacy of oral immunization with Edwardsiella tarda ghosts against edwardsiellosis in olive flounder (Paralichthys olivaceus). Aquaculture 269: 84-88. https://doi.org/10.1016/j.aquaculture.2007.04.018
  7. Baeck GW, Kim JH, Gomez DK, Park SC. 2006. Isolation and characterization of Streptococcus sp. from diseased flounder (Paralichthys olivaceus) in Jeju Island. J. Vet. Sci. 7: 53-58. https://doi.org/10.4142/jvs.2006.7.1.53
  8. Facklam R, Elliott J, Shewmaker L, Reingold A. 2005. Identification and characterization of sporadic isolates of Streptococcus iniae isolated from humans. J. Clin. Microbiol. 43: 933-937. https://doi.org/10.1128/JCM.43.2.933-937.2005
  9. Ye JD, Wang K, Li FD, Sun YZ. 2011. Single and combined effects of fructo- and mannan oligosaccharide supplements and Bacillus clausii on the growth, feed utilization, body composition, digestive enzyme activity, innate immune response and lipid metabolism of Japanese flounder Paralichthys olivaceus. Aquacult. Nutr. 17: e902-e911. https://doi.org/10.1111/j.1365-2095.2011.00863.x
  10. Rahimnejad S, Guardiola FA, Leclercq E, Esteban MÁ, Castex M, Sotoudeh E, et al. 2018. Effects of dietary supplementation with Pediococcus acidilactici MA18/5M, galactooligosaccharide and their synbiotic on growth, innate immunity and disease resistance of rockfish (Sebastes schlegeli). Aquaculture 482: 36-44. https://doi.org/10.1016/j.aquaculture.2017.09.020
  11. Hasan MT, Jang WJ, Lee S, Kim KW, Lee BJ, Han HS, et al. 2018. Effect of ${\beta}$-glucooligosaccharides as a new prebiotic for dietary supplementation in olive flounder (Paralichthys olivaceus) aquaculture. Aquac. Res. 49: 1310-1319. https://doi.org/10.1111/are.13588
  12. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. 2014. Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastro. Hepat. 11: 506-514. https://doi.org/10.1038/nrgastro.2014.66
  13. Bari ML, Ukuku DO, Kawasaki T, Inatsu Y, Isshiki K, Kawamoto S. 2005. Combined efficacy of nisin and pediocin with sodium lactate, citric acid, phytic acid, and potassium sorbate and EDTA in reducing the Listeria monocytogenes population of inoculated fresh-cut produce. J. Food Protect. 68: 1381-1387. https://doi.org/10.4315/0362-028X-68.7.1381
  14. Kim D, Beck BR, Heo SB, Kim J, Kim HD, Lee SM, et al. 2013. Lactococcus lactis BFE920 activates the innate immune system of olive flounder (Paralichthys olivaceus), resulting in protection against Streptococcus iniae infection and enhancing feed efficiency and weight gain in large-scale field studies. Fish Shellfish Immunol. 35: 1585-1590. https://doi.org/10.1016/j.fsi.2013.09.008
  15. Beck BR, Kim D, Jeon J, Lee SM, Kim HK, Kim OJ, et al. 2015. The effects of combined dietary probiotics Lactococcus lactis BFE920 and Lactobacillus plantarum FGL0001 on innate immunity and disease resistance in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 42: 177-183. https://doi.org/10.1016/j.fsi.2014.10.035
  16. Vergara CMDAC, Honorato TL, Maia GA, Rodrigues S. 2010. Prebiotic effect of fermented cashew apple (Anacardium occidentale L) juice. LWT-Food Sci. Technol. 43: 141-145. https://doi.org/10.1016/j.lwt.2009.06.009
  17. Cerezuela R, Meseguer J, Esteban MA. 2011. Current knowledge in synbiotic use for fish aquaculture: a review. J. Aquac. Res. Dev. 1: 1-7.
  18. Bai SC, Kim KW. 1997. Effects of dietary animal protein sources on growth and body composition in Korean rockfish, Sebastes schlegeli. J. Aqua. 10: 7-85.
  19. AOAC 1995. Official Methods of Analysis, 16th ed. Association of Official Analytical Chemists, Arlington, VA, USA.
  20. Nikoskelainen S, Ouwehanda AC, Bylundb G, Salminena S, Liliusa EM. 2003. Immune enhancement in rainbow trout (Oncorhynchus mykiss) by potential probiotic bacteria (Lactobacillus rhamnosus). Fish Shellfish Immunol. 15: 443-452. https://doi.org/10.1016/S1050-4648(03)00023-8
  21. Ellis AE. 1990. Lysozyme Assays, pp. 101-103. In Stolen JS, Fletcher TC, Anderson DP, Roberson, B.S., Van MWB (eds.), Techniques in Fish Immunology, Fair Haven, SOS Publications, Fair Haven.
  22. Quade MJ, Roth JA. 1997. A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet. Immunol. Immunop. 58: 239-248. https://doi.org/10.1016/S0165-2427(97)00048-2
  23. Abid A, Davies SJ, Waines P, Emery M, Castex M, Gioacchini G, et al. 2013. Dietary synbiotic application modulates Atlantic salmon (Salmo salar) intestinal microbial communities and intestinal immunity. Fish Shellfish Immunol. 35: 1948-1956. https://doi.org/10.1016/j.fsi.2013.09.039
  24. Van DH, Doolgindachbaporn S, Suksri A. 2014. Effects of low molecular weight agar and Lactobacillus plantarum on growth performance, immunity, and disease resistance of basa fish (Pangasius bocourti, Sauvage 1880). Fish Shellfish Immunol. 41: 340-345. https://doi.org/10.1016/j.fsi.2014.09.015
  25. Geraylou Z, Souffreau C, Rurangwa E, Meester LD, Courtin CM, Delcour JA, et al. 2013. Effects of dietary arabinoxylan-oligosaccharides (AXOS) and endogenous probiotics on the growth performance, non-specific immunity and gut microbiota of juvenile Siberian sturgeon (Acipenser baerii). Fish Shellfish Immunol. 35: 766-775. https://doi.org/10.1016/j.fsi.2013.06.014
  26. Maslowski KM, Mackay CR. 2011. Diet, gut microbiota and immune responses. Nat. Immunol. 12: 5-9.
  27. Satyanarayana U, Kumar AN, NaiduJN, Prasad DKV. 2014. Antioxidant supplementation for health-a boon or a bane? J. Dr. NTR Univ. Health Sci. 3: 221-230. https://doi.org/10.4103/2277-8632.146595
  28. Kim YR, Kim EY, Choi SY, Hossain MT, Oh R, Heo WS, et al. 2012. Effect of a probiotic strain, Enterococcus faecium, on the immune responses of olive flounder (Paralichthys olivaceus). J. Microbiol. Biotechnol. 22: 526-529. https://doi.org/10.4014/jmb.1108.08047
  29. Reece JB, Urry LA, Cain ML, Wasserman SA, Minorsky PV, Jackson R. 2014. The immune system, pp. 37-47, 9th Ed. Published by Benjamin Cummings, Pearson, Boston, USA.
  30. Geng X, Dong XH, Tan BP, Yang QH, Chi SY, Liu HY, et al. 2011. Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish Shellfish Immunol. 31: 400-406. https://doi.org/10.1016/j.fsi.2011.06.006
  31. Hoseinifar SH, Mirvaghefi A, Amoozegar MA, Sharifian M, Esteban MA. 2015. Modulation of innate immune response, mucosal parameters and disease resistance in rainbow trout (Oncorhynchus mykiss) upon synbiotic feeding. Fish Shellfish Immunol. 45: 27-32. https://doi.org/10.1016/j.fsi.2015.03.029
  32. Ai Q, Xu H, Mai K, Xu W, Wang J, Zhang W. 2011. Effects of dietary supplementation of Bacillus subtilis and fructooligosaccharide on growth performance, survival, non-specific immune response and disease resistance of juvenile large yellow croaker, Larimichthys crocea. Aquaculture 317: 155-161. https://doi.org/10.1016/j.aquaculture.2011.04.036
  33. Standen BT, Rawling MD, Davies SJ, Castex M, Foey A, Gioacchini G, et al. 2013. Probiotic Pediococcusacidilactici modulates both localised intestinal-and peripheral-immunity in tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 35: 1097-1104. https://doi.org/10.1016/j.fsi.2013.07.018
  34. Kim H, Jung BJ, Jung JH, Kim JY, Chung SK, Chung DK. 2012. Lactobacillus plantarum lipoteichoic acid alleviates TNF-${\alpha}$-induced inflammation in the HT-29 intestinal epithelial cell line. Mol. Cells 33: 479-486. https://doi.org/10.1007/s10059-012-2266-5
  35. Dziarski R. 1991. Demonstration of peptidoglycan-binding sites on lymphocytes and macrophages by photoaffinity cross-linking. J. Biol. Chem. 266: 4713-4718.
  36. Li W, Pan X, Cheng W, Cheng Y, Yin Y, Chen J, et al. 2018. Serum biochemistry, histology and transcriptome profile analysis reflects liver inflammation and damage following dietary histamine supplementation in yellow catfish (Pelteobagrus fulvidraco). Fish Shellfish Immunol. 77: 83-90. https://doi.org/10.1016/j.fsi.2018.03.036
  37. Lieschke GH, Trede NS. 2009. Fish immunology. Curr. Biol. 19: 678-682. https://doi.org/10.1016/j.cub.2009.06.068
  38. Marin ML, Lee JH, Murtha J, Ustunol Z, Pestka JJ. 1997. Differential cytokine production in clonal macrophage and T-cell lines cultured with bifidobacteria. J. Dairy Sci. 80: 2713-2720. https://doi.org/10.3168/jds.S0022-0302(97)76232-5
  39. Guzman-Villanueva LT, Tovar-Ramirez D, Gisbert E, Cordero H, Guardiola FA, Cuesta A, et al. 2014. Dietary administration of ${\beta}$-1, 3/1, 6-glucan and probiotic strain Shewanella putrefaciens, single or combined, on gilthead seabream growth, immune responses and gene expression. Fish Shellfish Immunol. 39: 34-41. https://doi.org/10.1016/j.fsi.2014.04.024
  40. Zhou QC, Buentello JA, Gatlin DM. 2010. Effects of dietary prebiotics on growth performance, immune response and intestinal morphology of red drum (Sciaenops ocellatus). Aquaculture 309: 253-257. https://doi.org/10.1016/j.aquaculture.2010.09.003
  41. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. 2011. The pro-and anti-inflammatory properties of the cytokine interleukin-6. BBA- Mol. Cell Res. 1813: 878-888.
  42. Dawood MAO, Koshio S, Ishikawa M, Yokoyama S, El- Basuini MF, Hossain MS, et al. 2016. Effects of dietary supplementation of Lactobacillus rhamnosus or/and Lactococcus lactis on the growth, gut microbiota and immune responses of red sea bream, Pagrus major. Fish Shellfish Immunol. 49: 275-285. https://doi.org/10.1016/j.fsi.2015.12.047
  43. Mehrabi Z, Firouzbakhsh F, Jafarpour A. 2012. Effects of dietary supplementation of synbiotic on growth performance, serum biochemical parameters and carcass composition in rainbow trout (Oncorhynchus mykiss) fingerlings. J. Anim. Physiol. An. N. 96: 474-481. https://doi.org/10.1111/j.1439-0396.2011.01167.x
  44. Ringo E. 2008. The ability of carnobacteria isolated from fish intestine to inhibit growth of fish pathogenic bacteria: a screening study. Aquac. Res. 39: 171-180. https://doi.org/10.1111/j.1365-2109.2007.01876.x

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