DOI QR코드

DOI QR Code

The Effects of a Dietary Edwardsiella tarda Specific Bacteriophage and Bacillus subtilis Mixture on Innate Immune Responses and Antibacterial Activity of Nile tilapia Oreochromis niloticus

Edwardsiella tarda의 특이 Bacteriophage와 Bacillus subtilis가 혼합된 사료급이가 나일 틸라피아(Oreochromis niloticus)의 선천적 면역반응과 항균효과에 미치는 영향

  • Baek, Min Suk (Department of Aquatic Life Medicine, Kunsan National University) ;
  • Hwang, Yo Sep (Department of Aquatic Life Medicine, Kunsan National University) ;
  • Choi, Sanghoon (Department of Aquatic Life Medicine, Kunsan National University)
  • 백민석 (군산대학교 수산생명의학과) ;
  • 황요셉 (군산대학교 수산생명의학과) ;
  • 최상훈 (군산대학교 수산생명의학과)
  • Received : 2013.10.04
  • Accepted : 2014.02.04
  • Published : 2014.02.28

Abstract

The present study investigated the effects of dietary Edwardsiella tarda (E. tarda) specific bacteriophage (phage) and Bacillus subtilis (B. subtilis) mixture on innate immune responses and antibacterial activity of Nile tilapia, Oreochromis niloticus. In a dietary experiment, tilapia were fed the control diet (C), a phage-only supplemented diet (P), a B. subtilis only supplemented diet (B), or a B. subtilis and phage mixed diet (B+P). A respiratory burst and significant increase in lysozyme activity (P<0.05) were noted in the B+P group, as compared to other groups after 4 days of feeding. The B group showed a significant (P<0.05) increase in respiratory burst and lysozyme activity versus the C and P groups, whereas no significant increases (P<0.05) were observed in the P and C groups. $ACH_{50}$ was significantly up-regulated in the B+P group versus other groups after 8 days of feeding (P<0.05). In vivo antibacterial activity was significantly enhanced in the B+P fed group, as compared to other groups (P<0.05) after 7 days of E. tarda challenge. A significant (P<0.05) increase in antibacterial activity was seen in the B group, as compared to C or P groups after 14 days of feeding. These results suggest that a B. subtilis and phage mixture could be utilized as an alternative to antibiotics in the control of fish diseases caused by E. tarda.

Keywords

References

  1. Abraham TJ, Babu CHS, Mondal S and Banerjee T. 2007. Effects of dietary supplementation of commercial human probiotic and antibiotic on the growth rate and content of intestinal microflora in ornamental fishes. Bangladesh J Fish Res 11, 57-63.
  2. Aly SM, Abdel-Galil Ahmed Y, Abdel-Aziz Ghareeb A and Mohamed MF. 2008. Studies on Bacillus subtilis and Lacto-bacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 25, 128-136. http://dx.doi.org/10.1016/j.fsi.2008.03.013.
  3. Baek MS, Hwang YS and Choi SH. 2013. Mixture of Edwardsiella tarda specific bacteriophage and Bacillus subtilis KM-1 enhanced bactericidal activity against Edwardsiella tarda. J Fish Pathol 26, 185-191. https://doi.org/10.7847/jfp.2013.26.3.185
  4. Bang JD, Chun SK, Park SI and Choi YJ. 1992. Studies on the biochemical and serological characteristics of Edwardsiella tarda isolated from cultured flounder, Paralichthys olivaceus. Fish Pathol 5, 29-35.
  5. Barrow P, Lovell M and Berchieri A. 1998. Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis inchickens and calves. Clin Diagn Lab Immunol 5, 294-298.
  6. Bizani D and Brandelli A. 2002. Characterization of a bacteriocin produced by a newly isolated Bacillus sp. strain 8A. J Appl Microbiol 93, 512-519. http://dx.doi.org/10.1046/j.1365-2672.2002.01720.x.
  7. Burr G, Gatlin D and Ricke S. 2005. Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture. J World Aquacult Soc 36, 425-436. http://dx.doi.org/10.1111/j.1749-7345.2005.tb00390.x.
  8. Carlton RM. 1999. Phage therapy: past history and future prospects. Immuno Ther Exp 47, 267-274.
  9. Cerezuela R, Guardiola FA, Meseguer J and Esteban MA. 2012. Increases in immune parameters by inulin and Bacillus subtilis dietary administration to gilthead seabream (Sparus aurata L.) did not correlate with disease resistance to Photobacterium damselae. Fish Shellfish Immunol 32, 1032-1040. http://dx.doi.org/10.1016/j.fsi.2012.02.025.
  10. Cha JH, Yang SY, Woo SH, Song JW, Oh DH and Lee KJ. 2012. Effects of dietary Supplementation with Bacillus sp. on growth performance, feed utilization, innate immunity and disease resistance against Streptococcus Iniae in olive flounder Paralichthys olivaceus. Kor J Fish Aquat Sci 45, 35-42. http://dx.doi.org/10.5657/KFAS.2012.0035.
  11. Chinabut S and Puttinaowarat S. 2005. The choice of disease control strategies to secure international market access for aquaculture products. Dev Biol 121, 255-261.
  12. Cutting SM. 2011. Bacillus probiotics. Food Microbiol 28, 214-220. https://doi.org/10.1016/j.fm.2010.03.007
  13. Ellis AE. 1999. Immunity to bacteria in fish. Fish Shellfish Immunol 9, 291-308. https://doi.org/10.1006/fsim.1998.0192
  14. Fuller R. 1989. probiotics in man and animals. J Appl Bacteriol 66, 365-378. https://doi.org/10.1111/j.1365-2672.1989.tb05105.x
  15. Geng X, Dong XH, Tan BP, Yang QH, Chi SY, Liu HY and Liu XQ. 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. http://dx.doi.org/10.1016/j.fsi.2011.06.006.
  16. Jolles P and Jolles J. 1984. What's new in lysozyme research? Always a model system, today as yesterday. Mol Cell Biochem 63, 165-189.
  17. Kanai K, Tawaki S and Uchida Y. 1988. An ecological study of Edwardsiella tarda in flounder farm. Fish Pathol 22, 41-47.
  18. Kumar R, Mukherjee SC, Ranjan R and Nayak SK. 2008. Enhanced innate immune parameters in Labeo rohita (Ham.) following oral administration of Bacillus subtilis. Fish Shellfish Immunol 24, 168-172. http://dx.doi.org/10.1016/j.fsi.2007.10.008.
  19. Kusuda R and Kawai K. 1998. Bacterial diseases of cultured marine fish in japan. Fish Pathol 33, 221-227. https://doi.org/10.3147/jsfp.33.221
  20. Lee CH, Heo YJ, Baek MS, Lee JU, Kang JY, Han MJ, Kyoung SB and Choi SH. 2011. Characterization of Edwardsiella tarda specific phage isolated from fish farms on west coast of Korea. J Fish Pathol 24, 85-93. http://dx.doi.org/10.7847/jfp.2011.24.2.085.
  21. Li JQ, Tan BP and Mai KS. 2009. Dietary probiotic Bacillus OJ and isomaltooligosaccharides influence the intestine microbial populations, immune responses and resistance to white spot syndrome virus in shrimp (Litopenaeus vannamei). Aquaculture 291, 35-40. http://dx.doi.org/10.1016/j.aquaculture.2009.03.005.
  22. Merrifield DL, Dimitroglou A, Bradley G, Baker RTM and Davies S J. 2010. Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) I. Effects on growth performance, feed utilization, intestinal microbiota and related health criteria. Aqua Nutr 16, 504-510. http://dx.doi.org/10.1111/j.1365-2095.2009.00689.x.
  23. Müller-Eberhard HJ. 1988. Molecular organization and function of the complement system. Ann Rev Biochem 57, 321-347. https://doi.org/10.1146/annurev.bi.57.070188.001541
  24. Nakai T, Sugimoto R, Park KH, Matsuoka S, Mori K, Nishioka T and Maruyama K. 1999. Protective effects of bacteriophage on experimental Lactococcus garvieae infection in yellowtail. Dis Aquat 37, 33-41. https://doi.org/10.3354/dao037033
  25. Nayak SK. 2010. Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29, 2-14. https://doi.org/10.1016/j.fsi.2010.02.017
  26. Nayak SK, Swain P and Mukherjee SC. 2007. Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp. Fish Shellfish Immunol 23, 892-896. http://dx.doi.org/10.1016/j.fsi.2007.02.008.
  27. Paek NS, Lim YB and Kim YM. 2001. Antibacterial Activity and Growth Promotion in Aquacultured Fish by Probiotics. Kor J Appl Microbiol Biotechnol 29, 56-61.
  28. Panigrahi A, Kiron V, Satoh S, Hirono I, Kobayashi T, Sugita H, Puangkaew J and Aoki T. 2007. Immune modulation and expression of cytokine genes in rainbow trout Oncorhynchus mykiss upon probiotic feeding. Dev Comp Immunol 31, 372-382. http://dx.doi.org/10.1016/j.dci.2006.07.004.
  29. Park SC, Ichiro S, Minoru F, Koh-Ichiro M and Toshihiro N. 2000. Isolation of Bacteriophage Specific to a Fish Pathogen, Pseudomonas plecoglossicida, as a Candidate for Disease Control. Applied and Environmental Microbiology, 1416-1422.
  30. Perdigon, G., Nader de macias, M. E., Alvarez, S., Oliver, G. and Pesce de Holgado, A. A. (1990) Prevention of gastrointestinal infection using immunobiological method with milk fermented with Lactobacillus casei and Lactobacillus acidophilus. J Dairy Res 57, 255-264. https://doi.org/10.1017/S002202990002687X
  31. Qi ZZ, Zhang XH, Boon N and Bossier P. 2009. Probiotics in aquaculture of China current state, problems and prospect. Aquaculture 290, 15-21. http://dx.doi.org/10.1016/j.aquaculture.2009.02.012.
  32. Rodgers CJ, Pringle JH, McCarthy DH and Austin B. 1981. Quantitative and qualitative studies of Aeromonas salmonicida bacteriophage. J Gen Microbiol 125, 335-345.
  33. Salinas I, Cuesta A, Esteban MA and Meseguer J. 2005. Dietary administration of Lactobacillus delbrueckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses. Fish Shellfish Immunol 19, 67-77. https://doi.org/10.1016/j.fsi.2004.11.007
  34. Salminen S, Ouwehand A, Benno Y and Lee YK. 1999. Probiotics:How should they be defined Trends. Food Sci Technol 10, 107-110. https://doi.org/10.1016/S0924-2244(99)00027-8
  35. Secombes CJ. 1990. Isolation of salmonid macrophages and analysis of their killing activity. In: Stolen J S, Fletcher T C, Anderson D P, Roberson B S, Van Muiswinkel W B, editors. Techniques in fish immunology. Fair, Haven, N.J, SOS Publications. 137-154.
  36. Shahani KM and Ayebo AD. 1980. Role of dietary lactobacilli in gastrointestinal microccology. Am J Clin Nutr 33, 2448-2457. https://doi.org/10.1093/ajcn/33.11.2448
  37. Sheikhzadeh N, Karimi Pashaki A, Nofouzi K, Heidarieh M and Tayefi-Nasrabadi H. 2012. Effects of dietary Ergosan on cutaneous mucosal immune response in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 32, 407-410. http://dx.doi.org/10.1016/j.fsi.2011.11.028.
  38. Shida K, Makino K, Morishita A, Takamizawa K, Hachimura S, Ametani A, Sato T, Kumagai Y, Habu S and Kaminogawa S. 1980. Lactobacilli in gastrointestinal microecology. Am J Clin Nutri 33, 2448-2457. https://doi.org/10.1093/ajcn/33.11.2448
  39. Smith HW and Huggins MB. 1980. The association of the O18, K1 and H7 antigens and the Co1V plasmid of a strain of Escherichia coli with its virulence and immunogenicity. J Gen Microbiol 128, 387-400.
  40. Smith HW and Huggins MB. 1982. Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics. J Gen Microbiol 128, 307-318.
  41. Soothill JS. 1992. Treatment of experimental infections of mice with bacteriophages. J Med Microbiol 37, 258-261. https://doi.org/10.1099/00222615-37-4-258
  42. Soothill JS. 1994. Bacteriophage prevents destruction of skin grafts by Pseudomonas aeruginosa. Burns 20, 209-211. https://doi.org/10.1016/0305-4179(94)90184-8
  43. Sulakvelidze A, Alavidze Z and Morris JG. 2001. Bacteriophage therapy. Antimicrob Agents Chemother 45, 649-659. https://doi.org/10.1128/AAC.45.3.649-659.2001
  44. Stevenson RMW and Airdrie DW. 1984. Isolation of Yersinia ruckeri bacteriophages. Appl Environ Microbiol 47, 1201-1205.
  45. Sun YZ, Yang HL, Ma RL and Lin WY. 2010. Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish Shellfish Immunol 29, 803-809. http://dx.doi.org/10.1016/j.fsi.2010.07.018.
  46. Tseng DY, Ho PY, Huang SY, Cheng SC, Shiu YL, Chiu CS and Liu CH. 2009. Enhancement of immunity and disease resistance in the white shrimp, Litopenaeus vannamei, by the probiotic, Bacillus subtilis E20. Fish Shellfish Immunol 26, 339-344. http://dx.doi.org/10.1016/j.fsi.2008.12.2003.
  47. Wang Y, Tian Z, Yao j and Li W. 2008. Effect of probiotics, Enterococcus faecium, on tilapia (Oreochromis niloticus) growth performance and immune response. Aquaculture 277, 203-207. http://dx.doi.org/10.1016/j.aquaculture.2008.03.007.
  48. Yano T. 1992. Assay of hemolytic complement activity. In: Stolen J S, Fletcher T C, Anderson D P, Hattari S C, Rowley A F, editors. Techniques in fish Immunology. SOS Publications, New Jersey, U.S.A., 131-141.
  49. Zhang Q, Ma H, Mai K, Zhang W, Liufu Z and Xu W. 2010. Interaction of dietary Bacillus subtilis and fructooligosaccharide on the growth performance, non-specific immunity of sea cucumber, Apostichopus japonicus. Fish Shellfish Immunol 29, 204-211. https://doi.org/10.1016/j.fsi.2010.03.009
  50. Zhao Y, Zhang W, Xu W, Mai K, Zhang Y and Liufu Z. 2012. Effects of potential probiotic Bacillus subtilis T13 on growth, immunity and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus. Fish Shellfish Immunol 32, 750-755. http://dx.doi.org/10.1016/j.fsi.2012.01.027.
  51. Zheng G, Yan LZ, Vederas JC and Zuber P. 1999. Genes of the sbo-alb locus of Bacillus subtilis are required for production of the antilisterial bacteriocin subtilosin. J Bacteriol 181, 7346-7355.