DOI QR코드

DOI QR Code

Effects of Fermented Sparassis crispa Stipe Extract Supplemented Diet on the Immune Responses of Philippines Eel, Anguilla bicolor

꽃송이버섯 기부 발효물 첨가 사료가 장어의 면역반응에 미치는 영향

  • Received : 2017.06.28
  • Accepted : 2017.08.25
  • Published : 2017.10.31

Abstract

This study examined the immune response of Philippines eel (Anguilla bicolor) to the oral administration of fermented Sparassis crispa stipe extract for 6 weeks. The S. crispa extract fermented with Lactobacillus plantarum showed a higher total phenol content (301.68 ppm) and DPPH radical scavenging activity (63.9%) than those fermented with other strains. Therefore, L. plantarum was selected as a suitable starter culture for the fermentation of S. crispa stipe. The eels were fed a commercial diet supplemented with 1% of fermented S. crispa stipe extract for 6 weeks. The mortality rate of the eels fed the supplemented diet was significantly lower than those of the control after 6 weeks. The lysozyme activity of the serum was increased significantly (12.33 ${\rightarrow}$ 54.66 units) after 6 weeks in the eel fed supplemented diets of fermented S. crispa stipe. The serum of the eel fed the supplemented diet of the S. crispa stipe extract showed higher bactericidal activity. These results suggest that both the S. crispa stipe extract and fermented S. crispa stipe have strong potential to activate the innate immune response of the Philippines eel.

본 연구에서는 폐기되고 있는 꽃송이버섯 기부 발효에 적합한 균주 선발을 위해 Lactobacillus plantarum, Saccharomyces cerevisiae, Bacillus subtilis를 활용하여 발효를 진행하였으며, 생균수 실험 결과 L. plantarum이 발효 48시간에 1.486의 흡광도를 보여 빠른 발효속도와 생육능을 보였다. 총 페놀 함량은 L. plantarum과 S. cerevisiae를 활용하여 발효한 실험구에서 301.68 ppm, 299.35 ppm으로 발효 전보다 높은 함량을 보였으며, B. subtilis 발효 실험구는 큰 차이를 보이지 않았다. DPPH 라디칼 소거 활성은 L. plantarum이 63.9%로 가장 우수한 항산화 활성을 보여 L. plantarum을 이용하여 꽃송이버섯 기부를 발효한 후 장어에 사료 첨가제로 급이하였다. 6주간 장어의 폐사는 대조구에서 60마리로 가장 많은 폐사를 보였으며, 꽃송이버섯 기부 추출물이 24마리로 가장 적은 폐사를 보였다. 장어 혈청의 lysozyme 용균 활성 및 E. coli 살균능은 꽃송이버섯 기부 추출물과 발효물 모두 대조구에 비해 높은 활성을 보였다.

Keywords

References

  1. Kim HY, Shin JW, Sim GC, Park HO, Kim HS, Kim SM, Cho JS, Jang YM. 2000. Comparison of the taste compounds of wild and cultured eel, puffer and snake head. Korean J Food Sci Technol 32: 1058-1067.
  2. Kim DJ, Lee NS, Kim SK, Lee BI, Seong KB, Kim KK. 2013. Effects of water temperature and estradiol-$17{\beta}$ on the sex ratio and growth of the Japanese eel, Anguilla japonica. J Life Sci 23: 1454-1459. https://doi.org/10.5352/JLS.2013.23.12.1454
  3. Miller MJ. 2003. The worldwide distribution of Anguillid leptocephali. In Eel Biology. Aida K, Tsukamoto K, Yamauchi K, eds. Springer-Verlag, Tokyo, Japan. p 157-168.
  4. Cho HS, Choi JH, Ko HB, Seo JS, Ahn JC. 2011. Evaluation of major nutrients of domestic farmed eels Anguilla japonica. Korean J Fish Aquat Sci 44: 237-242.
  5. Ahn JC, Chong WS, Na JH, Yun HB, Shin KJ, Lee KW, Park JT. 2015. An evaluation of major nutrients of four farmed freshwater eel species (Anguilla japonica, A. rostrata, A. bicolor pacifica and A. marmorata). Korean J Fish Aquat Sci 48: 44-50.
  6. Kim WS, Ok HN, Kim DH, Kim HY, Oh MJ. 2011. Current status of pathogen infection in cultured eel Anguilla japonica between 2000 and 2010. J Fish Pathol 24: 237-245. https://doi.org/10.7847/jfp.2011.24.3.237
  7. Chun SK. 1988. Detection and control of bacterial diseases of cultured fishes in Korea. J Fish Pathol 1: 5-30.
  8. Kim YG, Kim EB, Kim JY, Chun SK. 1989. Studies on a Nematode, Anguillicola crassa parasitic in the air bladder of the eel. J Fish Pathol 2: 1-18.
  9. Han JJ, Park SW, Kim YG. 2000. Studies on monogenean trematodes classification from cultured freshwater fishes in Korea 1. Monogenean trematodes from Anguilla japonica and Parasilurus asotus. J Fish Pathol 13: 75-86.
  10. Joh SJ, Kwon YK, Kim MC, Kim MJ, Kwon HM, Park JW, Kwon JH, Kim JH. 2007. Heterosporis anguillarum infections in farm cultured eels (Anguilla japonica) in Korea. J Vet Sci 8: 147-149. https://doi.org/10.4142/jvs.2007.8.2.147
  11. Yang HC, Chun SK. 1991. On the histopathological changes and methemoglobinemia to nitrite toxicity in the culture farms of eel, Anguilla japonica. J Fish Pathol 4: 1-13.
  12. Kim MS, Yang HC. 1996. Histopathological study of acute toxicity of ammonia to the eel, Anguilla japonica in high temperature and pH levels. J Fish Pathol 9: 147-155.
  13. Jo MR, Park KBW, Lee HJ, Kim JH, Lee TS, Jung SH, Lee DS, Yoon HD, Kim PH. 2010. Distribution of fluoroquinolones in the carp (Cyprinus carpio) and eel (Anguilla japonica) following their oral administration. Korean J Fish Aquat Sci 43: 623-628.
  14. Lee YG, Thi NN, Kim HG, Lee DY, Lee SE, Kim GS, Baek NI. 2016. Ergosterol peroxides from the fruit body of Sparassis crispa. J Appl Biol Chem 59: 313-316.
  15. Kim IK, Yun YC, Shin YC, Yoo J. 2013. Effect of Sparassis crispa extracts on immune cell activation and tumor growth inhibition. J Life Sci 23: 984-988. https://doi.org/10.5352/JLS.2013.23.8.984
  16. Choi WS, Shin PG, Bok YY, Jun NH, Kim GD. 2013. Anti-inflammatory effects of Sparassis crispa extracts. J Mushrooms 11: 46-51. https://doi.org/10.14480/JM.2013.11.1.046
  17. Guillamon E, Garcia-Lafuente A, Lozano M, D'Arrigo M, Rostagno MA, Villares A, Martinez JA. 2010. Edible mushrooms: Role in the prevention of cardiovascular diseases. Fitoterapia 81: 715-723. https://doi.org/10.1016/j.fitote.2010.06.005
  18. Kim HS, Kim JY, Ryu HS, Park HG, Kim YO, Kang JS, Kim HM, Hong JT, Kim Y, Han SB. 2010. Induction of dendritic cell maturation by ${\beta}$-glucan isolated from Sparassis crispa. Int Immunopharmacol 10: 1284-1294. https://doi.org/10.1016/j.intimp.2010.07.012
  19. Seo SH, Park SE, Moon YS, Lee YM, Na CS, Soon HS. 2016. Component analysis and immuno-stimulating activity of Sparassis crispa stipe. Korean J Food Sci Technol 48: 515-520. https://doi.org/10.9721/KJFST.2016.48.5.515
  20. Cheong JC, Park JS, Hong IP, Seok SJ, Jhune CS, Lee CJ. 2008. Cultural characteristics of cauliflower mushroom, Sparassis crispa. Korean J Mycol 36: 16-21. https://doi.org/10.4489/KJM.2008.36.1.016
  21. Kim SY, Shin KS, Lee H. 2004. Immunopotentiating activities of cellular components of Lactobacillus brevis FSB-1. J Korean Soc Food Sci Nutr 33: 1552-1559. https://doi.org/10.3746/jkfn.2004.33.9.1552
  22. Park SH, Kim YA, Lee DK, Lee S, Chung MJ, Kang BY, Kim K, Ha NJ. 2007. Antibacterial activity and macrophage activation of lactic acid bacteria. J Environ Toxicol 22: 287-297. https://doi.org/10.1002/tox.20254
  23. AOAC. 1980. Official methods of analysis. 14th ed. Association of Official Analytical Chemists, Washington, DC, USA. p 31.
  24. Blois MS. 1958. Antioxidant determinations by the use of a stable free radical. Nature 181: 1199-1200. https://doi.org/10.1038/1811199a0
  25. Kim JD, Woo SH, Kim YC, Lee JH, Cho YC, Choi SM, Park SI. 2008. The effects of yeast ${\beta}$-glucan in the diet on immune response of Japanese eel, Anguilla japonica, by oral administration. J Fish Pathol 21: 219-228.
  26. Yoo BH, Park SI, Chun SK. 1992. Bactericidal action by complement of fish serum. J Fish Pathol 5: 9-18.
  27. Hong MH, Jin YJ, Pyo YH. 2012. Antioxidant properties and ubiquinone contents in different parts of several commercial mushrooms. J Korean Soc Food Sci Nutr 41: 1235-1241. https://doi.org/10.3746/jkfn.2012.41.9.1235
  28. Barros L, Ferreira MJ, Queiros B, Ferreira ICFR, Baptista P. 2007. Total phenols, ascorbic acid, ${\beta}$-carotene and lycopene in Portuguese wild edible mushrooms and their antioxidant activities. Food Chem 103: 413-419. https://doi.org/10.1016/j.foodchem.2006.07.038
  29. Nowacka N, Nowak R, Drozd M, Olech M, Los R, Malm A. 2014. Analysis of phenolic constituents, antiradical and antimicrobial activity of edible mushrooms growing wild in Poland. LWT-Food Sci Technol 59: 689-694. https://doi.org/10.1016/j.lwt.2014.05.041
  30. Rodriguez H, Landete JM, de las Rivas B, Munoz R. 2008. Metabolism of food phenolic acids by Lactobacillus plantarum CECT $748^T$. Food Chem 107: 1393-1398. https://doi.org/10.1016/j.foodchem.2007.09.067
  31. Osawa R, Kuroiso K, Goto S, Shimizu A. 2000. Isolation of tannin-degrading lactobacilli from humans and fermented foods. J Appl Environ Microbiol 66: 3093-3097. https://doi.org/10.1128/AEM.66.7.3093-3097.2000
  32. Lee JJ, Son HY, Choi YM, Cho JH, Min JK, Oh HK. 2016. Physicochemical components and antioxidant activity of Sparassis crispa mixture fermented by lactic acid bacteria. Korean J Food Preserv 23: 361-368. https://doi.org/10.11002/kjfp.2016.23.3.361
  33. Hernandez T, Estrella I, Perez-Gordo M, Alegria EG, Tenorio C, Ruiz-Larrrea F, Moreno-Arribas MV. 2007. Contribution of malolactic fermentation by Oenococcus oeni and Lactobacillus plantarum to the changes in the nonanthocyanin polyphenolic composition of red wine. J Agric Food Chem 55: 5260-5266. https://doi.org/10.1021/jf063638o
  34. Escudero-Lopez B, Cerrillo I, Herrero-Martin G, Hornero-Mendez D, Gil-Izquierdo A, Medina S, Ferreres F, Berna G, Martin F, Fernandez-Pachon MS. 2013. Fermented orange juice: source of higher carotenoid and flavanone contents. J Agric Food Chem 61: 8773-8782. https://doi.org/10.1021/jf401240p
  35. Park SE, Seo SH, Moon YS, Lee YM, Na CS, Son HS. 2016. Antioxidant and immunological activities of Sparassis crispa fermented with Meyerozyma guilliermondii FM. J Korean Soc Food Sci Nutr 45: 1398-1405. https://doi.org/10.3746/jkfn.2016.45.10.1398
  36. Rodriguez H, Curiel JA, Landete JM, de las Rivas B, de Felipe FL, Gomez-Cordoves C, Mancheno JM, Munoz R. 2009. Food phenolics and lactic acid bacteria. Int J Food Microbiol 132: 79-90. https://doi.org/10.1016/j.ijfoodmicro.2009.03.025
  37. Yang HS, Choi YJ, Oh HH, Moon JS, Jung HK, Kim KJ, Choi BS, Lee JW, Huh CK. 2014. Antioxidative activity of mushroom water extracts fermented by lactic acid bacteria. J Korean Soc Food Sci Nutr 43: 80-85. https://doi.org/10.3746/jkfn.2014.43.1.080
  38. Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Niu C, Yang Z, Wang Q. 2012. Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem 135: 1914-1919. https://doi.org/10.1016/j.foodchem.2012.06.048
  39. Lin MY, Yen CL. 1999. Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47: 1460-1466. https://doi.org/10.1021/jf981149l
  40. Lee J, Hwang KT, Chung MY, Cho DH, Park CS. 2005. Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect. Food Sci 70: m388-m391. https://doi.org/10.1111/j.1365-2621.2005.tb11524.x
  41. Jeon GH, Cho SH, Kim HS, Myung SH, Kim HJ, Jung WG, Park BH, Lee KJ. 2013. Effects of the inclusion of Kimchi lactic acid bacterial culture in extruded pellets on the growth, body composition and immune response of Juvenile olive flounder Paralichthys olivaceus. Korean J Fish Aquat Sci 46: 552-558.
  42. Shibata A, Hida TH, Ishibashi KI, Miura NN, Adachi Y, Ohno N. 2012. Disruption of actin cytoskeleton enhanced cytokine synthesis of splenocytes stimulated with beta-glucan from the cauliflower medicinal mushroom, Sparassis crispa Wulf.:Fr. (higher basidiomycetes) in vitro. Int J Med Mushrooms 14: 257-269. https://doi.org/10.1615/IntJMedMushr.v14.i3.30
  43. Harada T, Miura N, Adachi Y, Nakajima M, Yadomae T, Ohno N. 2002. Effect of SCG, 1,3-${\beta}$-D-glucan from Sparassis crispa on the hematopoietic response in cyclophosphamide induced leukopenic mice. Biol Pharm Bull 25: 931-939. https://doi.org/10.1248/bpb.25.931
  44. Nam HJ, Park KI, Choi MS. 2014. Effects of propolis extracts on the immune response in cultured flounder, Paralichthys olivaceus. J Fish Pathol 27: 47-56. https://doi.org/10.7847/jfp.2014.27.1.047
  45. Kim MC, Kim MJ, Kim JS, Heo MS. 2007. Effect of culture broth from mushroom mycelium on growth and non-specific immune parameters in flounder (Paralichthys olivaceus) by oral administration. J Life Sci 17: 1434-1440. https://doi.org/10.5352/JLS.2007.17.10.1434
  46. Jhon BK, Kim MC, Kim YH, Heo MS. 2009. Effects of the culture broth of lactic acid bacteria cultured in herb extracts on growth promotion and nonspecific immune responses of aquacultured fish. J Life Sci 19: 87-93. https://doi.org/10.5352/JLS.2009.19.1.087
  47. Park JW, Kim T, Lim DJ, Lee HB, Joo YS, Park YI. 2004. Antibacterial activities of mushroom liquid culture extracts against livestock disease-causing bacteria and antibiotic resistant bacteria. Korean J Mycol 32: 145-147. https://doi.org/10.4489/KJM.2004.32.2.145
  48. Alakomi HL, Skytta E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM. 2000. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. J Appl Environ Microbiol 66: 2001-2005. https://doi.org/10.1128/AEM.66.5.2001-2005.2000