생명과학회지 (Journal of Life Science)

  • 제27권6호
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  • Pages.652-660
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  • 2017
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  • 1225-9918(pISSN)
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  • 2287-3406(eISSN)
한국생명과학회 (Korean Society of Life Science)
권호 표지
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양어 사료첨가제로서의 유산균 발효 개똥쑥의 항산화 및 항균활성

Antioxidant and Antibacterial Activities of Lactobacillus-fermented Artemisia annua L. as a Potential Fish Feed Additive

  • 이아란 (건국대학교 동물자원과학과) ;
  • 우개민 (건국대학교 동물자원과학과) ;
  • 강수경 (건국대학교 축산식품공학과) ;
  • 한성구 (건국대학교 축산식품공학과) ;
  • 이봉주 (국립수산과학원 사료연구센터) ;
  • 김수기 (건국대학교 동물자원과학과)
  • Lee, Ah-Ran (Department of Animal Science and Technology, Konkuk University) ;
  • Niu, Kai-Min (Department of Animal Science and Technology, Konkuk University) ;
  • Kang, Su-Kyung (Department of Food Science of Animal Resource, Konkuk University) ;
  • Han, Sung-Gu (Department of Food Science of Animal Resource, Konkuk University) ;
  • Lee, Bong-Joo (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Kim, Soo-Ki (Department of Animal Science and Technology, Konkuk University)
  • 투고 : 2017.01.02
  • 심사 : 2017.02.15
  • 발행 : 2017.06.30
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초록

최근 양어에서는 전염병, 환경오염, 어분 가격 상승 등으로 어려움을 가지고 있다. 본 연구는 쑥에서 분리한 L. plantarum SK3494를 이용하여 전통 약초인 개똥쑥을 발효시켜 in vitro 생리활성을 측정하고 어류용 사료첨가제로서의 가능성을 연구하였다. 개똥쑥의 발효시 유산균수는 9.38 log10 CFU/ml이며, pH는 4.1로 나타났다. 발효개똥쑥의 항산화활성은 DPPH 측정과 MAC-T 세포 내 과산화물 감소 실험에서 뛰어난 효과를 보였다. 발효개똥쑥은 어류 병원균인Photobacterium damselae subsp. damselae와 Vibrio ichthyoenteri에 대하여 강한 항균활성을 나타내었다. 따라서 유산균을 이용한 개똥쑥 발효물은 양식용 사료첨가제로써 가능성을 가지고 있는 것으로 판단되었다.

Fermented medical herbs using Lactobacilli have attracted significant attention due to their enhanced biological activities. A traditional medicinal plant, Artemisia annua L., was fermented using a probiotic strain, L. plantarum SK3494. The strain was isolated from Artemisia princeps var. orientalis and molecularly identified through sequence similarities and phylogenetic tree analysis. The antioxidant activity of L. plantarum-fermented A. annua L. (LFA) was determined using the DPPH free radical scavenging assay. Cellular antioxidant activity of LFA was examined using the superoxide radical reduction assay in MAT-C cells. Total polyphenol contents (TPC) and flavonoid contents (TFC) of LFA were determined. The antibacterial activity of LFA against fish pathogens was also determined in this study. The viable cell number (9.38 log10 CFU/ml) and pH (4.1) results showed good adaptive ability of the selected strain during fermentation. LFA was found to have enhanced antioxidant activity compared to non-fermented A. annua L. (NFA) based on the DPPH assay. Cellular antioxidant activity was present in both LFA and NFA. After 24 hr and 48 hr of fermentation, the LFA also showed antibacterial activities against fish pathogens Photobacterium damselae subsp. damselae and Vibrio ichthyoenteri. These results suggest that L. plantarum-fermented A. annua L. may have potential as a feed additive in aquaculture.

키워드

참고문헌

  1. Aftabuddin, S., Kashem, M. A., Kader, M. A., Sikder, M. and Hakim, M. A. 2013. Use of Streptomyces fradiae and Bacillus megaterium as probiotics in the experimental culture of tiger shrimp Penaeus monodon (Crustacea, Penaeidae). Aquac. Aquar. Conserv. Legis. 6, 253-267.
  2. Ahmed, S. T., Islam, M., Mun, H. S., Sim, H. J., Kim, Y. J. and Yang, C. J. 2014. Effects of Bacillus amyloliquefaciens as a probiotic strain on growth performance, cecal microflora, and fecal noxious gas emissions of broiler chickens. Poult Sci. 93, 1963-1971. https://doi.org/10.3382/ps.2013-03718
  3. Botes, M., van Reenen, C. A. and Dicks, L. M. 2008. Evaluation of Enterococcus mundtii ST4SA and Lactobacillus plantarum 423 as probiotics by using a gastro-intestinal model with infant milk formulations as substrate. Int. J. Food Microbiol. 128, 362-370. https://doi.org/10.1016/j.ijfoodmicro.2008.09.016
  4. Bourafa, N., Loucif, L., Boutefnouchet, N. and Rolain, J. M. 2015. Enterococcus hirae, an unusual pathogen in humans causing urinary tract infection in a patient with benign prostatic hyperplasia: first case report in Algeria. New Microbes New Infect. 8, 7-9. https://doi.org/10.1016/j.nmni.2015.08.003
  5. Boyanova, L., Gergova, G., Nikolov, R., Derejian, S., Lazarova, E., Katsarov, N, Ivan, M. and Krastev, Z. 2005. Activity of Bulgarian propolis against 94 Helicobacter pylori strains in vitro by agar-well diffusion, agar dilution and disc diffusion methods. J. Med. Microbiol. 54, 481-483. https://doi.org/10.1099/jmm.0.45880-0
  6. Brisibe, E. A., Umoren, U. E., Brisibe, F., Magalhäes, P. M., Ferreira, J. F., Luthria, D. and Prior, R. L. 2009. Nutritional characterisation and antioxidant capacity of different tissues of Artemisia annua L. Food Chem. 115, 1240-1246. https://doi.org/10.1016/j.foodchem.2009.01.033
  7. Chakraborty, S. B. and Hancz, C. 2011. Application of phytochemicals as immunostimulant, antipathogenic and antistress agents in finfish culture. Rev. Aquac. 3, 103-119. https://doi.org/10.1111/j.1753-5131.2011.01048.x
  8. Chakraborty, S. B., Horn, P. and Hancz, C. 2014. Application of phytochemicals as growth‐promoters and endocrine modulators in fish culture. Rev. Aquac. 6, 1-19. https://doi.org/10.1111/raq.12021
  9. Curiel, J. A., Pinto, D., Marzani, B., Filannino, P., Farris, G. A., Gobbetti, M. and Rizzello, C. G. 2015. Lactic acid fermentation as a tool to enhance the antioxidant properties of Myrtuscommunisberries. Microb. Cell. Fact. 14, 1. https://doi.org/10.1186/s12934-014-0183-3
  10. Cutting, S. M. 2011. Bacillus probiotics. Food Microbiol. 28, 214-220. https://doi.org/10.1016/j.fm.2010.03.007
  11. da Mota, F. F., Vollú, R. E., Jurelevicius, D. and Seldin, L. 2016. Whole-genome sequence of Rummeliibacillus stabekisii strain PP9 isolated from Antarctic soil. Genome Announc. 4, e00416-16.
  12. Dong, J. W., Cai, L., Xiong, J., Chen, X. H., Wang, W. Y., Shen, N. and Ding, Z. T. 2015. Improving the antioxidant and antibacterial activities of fermented Bletillastriata with Fusariumavenaceum and Fusariumoxysporum. Process Biochem. 50, 8-13. https://doi.org/10.1016/j.procbio.2014.09.008
  13. Dutkiewicz, J., Mackiewicz, B., Kinga Lemieszek, M., Golec, M. and Milanowski, J. 2016. Pantoea agglomerans: a mysterious bacterium of evil and good. Part III. Deleterious effects: infections of humans, animals and plants. Ann. Agric. Environ. Med. 23, 197-205. https://doi.org/10.5604/12321966.1203878
  14. El-Shafei, K., Sharaf, M., Ibrahim, A., Sadek, I. and El-Sayed, S. 2013. Evaluation of Lactobacillus plantarum as a probiotic in aquaculture: Emphasis on growth performance and innate immunity. J. Appl. Sci. Res. 9, 572-582.
  15. Giraffa, G., Chanishvili, N. and Widyastuti, Y. 2010. Importance of lactobacilli in food and feed biotechnology. Res. Microbiol. 161, 480-487. https://doi.org/10.1016/j.resmic.2010.03.001
  16. Han, S. G., Newsome, B. and Hennig, B. 2013. Titanium dioxide nanoparticles increase inflammatory responses in vascular endothelial cells. Toxicology 306, 1-8. https://doi.org/10.1016/j.tox.2013.01.014
  17. Herigstad, B., Hamilton, M. and Heersink, J. 2001. How to optimize the drop plate method for enumerating bacteria. J. Microbiol. Methods 44, 121-129. https://doi.org/10.1016/S0167-7012(00)00241-4
  18. Higashide, T., Takahashi, M., Kobayashi, A., Ohkubo, S., Sakurai, M., Shirao, Y., Tamura, T. and Sugiyama, K. 2005. Endophthalmitis caused by Enterococcus mundtii. J. Clin. Microbiol. 43, 1475-1476. https://doi.org/10.1128/JCM.43.3.1475-1476.2005
  19. Hixson, S. M. 2014. Fish nutrition and current issues in aquaculture: the balance in providing safe and nutritious seafood, in an environmentally sustainable manner. J. Aquac Res. Dev. 5, 1.
  20. Hong, H., Niu, K. M., Lee, J. H., Cho, S., Han, S. G. and Kim, S. K. 2016. Characteristics of Chinese chives (Allium tuberosum) fermented by Leuconostoc mesenteroides. Appl. Biol. Chem. 59, 349-357. https://doi.org/10.1007/s13765-016-0166-7
  21. Huynh, H. T., Robitaille, G. and Turner, J. D. 1991. Establishment of bovine mammary epithelial cells (MAC-T): an in vitro model for bovine lactation. Exp. Cell Res. 197, 191-199. https://doi.org/10.1016/0014-4827(91)90422-Q
  22. Huynh, N. T., Van Camp, J., Smagghe, G. and Raes, K. 2014. Improved release and metabolism of flavonoids by steered fermentation processes: a review. Int. J. Mol Sci. 15, 19369- 19388. https://doi.org/10.3390/ijms151119369
  23. Ibrahim, N. A., Mustafa, S. and Ismail, A. 2014. Effect of lactic fermentation on the antioxidant capacity of Malaysian herbal teas. Int. Food Res. J. 21, 1483-1488.
  24. Iqbal, S., Younas, U., Chan, K. W., Zia-Ul-Haq, M. and Ismail, M. 2012. Chemical composition of Artemisia annua L. leaves and antioxidant potential of extracts as a function of extraction solvents. Molecules 17, 6020-6032. https://doi.org/10.3390/molecules17056020
  25. Kagkli, D. M.,Corich, V., Bovo, B., Lante, A. and Giacomini, A. 2016. Antiradical and antimicrobial properties of fermented red chicory (Cichoriumintybus L.) by-products. Ann. Microbiol. 66, 1377-1386. https://doi.org/10.1007/s13213-016-1225-3
  26. Kang, C. H., Shin, Y., Kim, Y. and So, J. S. 2016. Isolation of Lactobacillus strains from shellfish for their potential use as probiotics. Biotechnol. Bioprocess Eng. 21, 46-52. https://doi.org/10.1007/s12257-015-0518-x
  27. Kim, C. H., Kim, G. B., Chang, M. B., Bae, G. S., Paik, I. K. and Kil, D. Y. 2012. Effect of dietary supplementation of Lactobacillus-fermented Artemisia princeps on growth performance, meat lipid peroxidation, and intestinal microflora in Hy-line Brown male chickens. Poult. Sci. 91, 2845-2851. https://doi.org/10.3382/ps.2012-02467
  28. Kim, D. W., Kim, J. H., Kang, G. H., Kang, H. K., Park, S. B., Park, J. H., Bang, H. T., Kim, M. J., Na, J. C., Chae, H. S., Choi, H. C., Suh, O. S., Kim, S. H. and Kang, C. W. 2010. Studies for antibiotic free chicken production using water extracts from Artemisia capillaris and Camellia sinensis. Kor. J. Food Sci. Anim. Resour. 30, 975-988. https://doi.org/10.5851/kosfa.2010.30.6.975
  29. Kim, K. H., Yun, Y. S., Chun, S. Y. and Yook, H. S. 2012. Antioxidant and antibacterial activities of grape pomace fermented by various microorganisms. J. Kor. Soc. Food Sci. Nutr. 41, 1049-1056. https://doi.org/10.3746/jkfn.2012.41.8.1049
  30. Kim, W. S., Choi, W. J., Lee, S., Kim, W. J., Lee, D. C., Sohn, U. D., Shin, H. S. and Kim, W. 2015. Anti-inflammatory, antioxidant and antimicrobial effects of artemisinin extracts from Artemisia annua L. Kor. J. Physiol. Pharmacol. 19, 21-27.
  31. Lai, C. C., Tan, C. K., Lin, S. H., Liu, W. L., Liao, C. H., Huang, Y. T. and Hsueh, P. R. 2010. Bacteraemia caused by non-freundii, non-koseri Citrobacter species in Taiwan. J. Hosp. Infect. 76, 332-335. https://doi.org/10.1016/j.jhin.2010.06.006
  32. Landete, J. M., Curiel, J. A., Rodríguez, H., de las Rivas, B. and Munoz, R. 2008. Study of the inhibitory activity of phenolic compounds found in olive products and their degradation by Lactobacillus plantarum strains. Food Chem. 107, 320-326. https://doi.org/10.1016/j.foodchem.2007.08.043
  33. Lee, Y. E., Kang, I. J., Yu, E. A., Kim, S. and Lee, H. J. 2012. Effect of feeding the combination with Lactobacillus plantarum and Bacillus subtilis on fecal microflora and diarrhea incidence of Korean native calves. Kor. J. Vet. Serv. 35, 343-346. https://doi.org/10.7853/kjvs.2012.35.4.343
  34. Li, S., Zhao, Y., Zhang, L., Zhang, X., Huang, L., Li, D. and 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
  35. Ljungh, A. and Wadstrom, T. 2006. Lactic acid bacteria as probiotics. Curr. Issues Intest. Microbiol. 7, 73-90.
  36. Makras, L., Triantafyllou, V., Fayol-Messaoudi, D., Adriany, T., Zoumpopoulou, G., Tsakalidou, E., Servin, A. and De Vuyst, L. 2006. Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella entericaserovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Res. Microbiol. 157, 241-247. https://doi.org/10.1016/j.resmic.2005.09.002
  37. Martinez Cruz, P., Ibanez, A. L., Monroy Hermosillo, O. A. and Ramirez Saad, H. C. 2012. Use of probiotics in aquaculture. ISRN Microbiol. 2012, doi:10.5402/2012/916845.
  38. Mishra, V., Shah, C., Mokashe, N., Chavan, R., Yadav, H. and Prajapati, J. 2015. Probiotics as potential antioxidants: a systematic review. J. Agric. Food Chem. 63, 3615-3626. https://doi.org/10.1021/jf506326t
  39. Moreno, M. I. N., Isla, M. I., Sampietro, A. R. and Vattuone, M. A. 2000. Comparison of the free radical-scavenging activity of propolis from several regions of Argentina. J. Ethnopharmacol. 71, 109-114. https://doi.org/10.1016/S0378-8741(99)00189-0
  40. Poirel, L., Figueiredo, S., Cattoir, V., Carattoli, A. and Nordmann, P. 2008. Acinetobacter radioresistens as a silent source of carbapenem resistance for Acinetobacter spp. Antimicrob. Agents Chemother. 52, 1252-1256. https://doi.org/10.1128/AAC.01304-07
  41. Rank, C. U., Kristensen, P. L., Hansen, D. S. and Brandi, L. 2016. Catheter related Escherichia hermannii sepsis in a haemodialysis patient. Open Microbiol. J. 10, 1-3. https://doi.org/10.2174/1874285801610010001
  42. Rath, K., Taxis, K., Walz, G., Gleiter, C. H., Li, S. M. and Heide, L. 2004. Pharmacokinetic study of artemisinin after oral intake of a traditional preparation of Artemisia annua L.(annual wormwood). Am. J. Trop. Med. Hyg. 70, 128-132.
  43. Rodriguez, H., Curiel, J. A., Landete, J. M., de las Rivas, B., de Felipe, F. L., Gomez-Cordoves, C., Mancheno, J. M. and 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
  44. Rodriguez, H., Landete, J. M., de las Rivas, B. and 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
  45. Roh, J. Y., Choi, J. Y., Li, M. S., Jin, B. R. and Je, Y. H. 2007. Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J. Microbiol. Biotechnol. 17, 547.
  46. Saeed, N., Khan, M. R. and Shabbir, M. 2012. Antioxidant activity, total phenolic and total flavonoid contents of whole plant extracts Torilisleptophylla L. BMC Complement Altern. Med. 12, 221-232. https://doi.org/10.1186/1472-6882-12-S1-P221
  47. Shen, X., Yi, D., Ni, X., Zeng, D., Jing, B., Lei, M., Bian, Z., Zeng, Y., Li, Tao. and Xin, J. 2014. Effects of Lactobacillus plantarum on production performance, immune characteristics, antioxidant status, and intestinal microflora of bursin- immunized broilers. Can. J. Microbiol. 60, 193-202. https://doi.org/10.1139/cjm-2013-0680
  48. Silva, T. F. A., Petrillo, T. R., Yunis-Aguinaga, J., Marcusso, P. F., da Silva Claudiano, G., de Moraes, F. R. and de Moraes, J. R. E. 2015. Effects of the probiotic Bacillus amyloliquefaciens on growth performance, hematology and intestinal morphometry in cage-reared Nile tilapia. Lat. Am. J. Aqua.t Res. 43, 963-971.
  49. Suo, C., Yin, Y., Wang, X., Lou, X., Song, D., Wang, X. and Gu, Q. 2012. Effects of lactobacillus plantarum ZJ316 on pig growth and pork quality. BMC Vet. Res. 8, 89. https://doi.org/10.1186/1746-6148-8-89
  50. Svensson, L., Sekwati-Monang, B., Lutz, D. L., Schieber, A. and Gaanzle, M. G. 2010. Phenolic acids and flavonoids in nonfermented and fermented red sorghum (Sorghum bicolor (L.) Moench). J. Agric. Food Chem. 58, 9214-9220. https://doi.org/10.1021/jf101504v
  51. Szkaradkiewicz, A., Chudzicka-Strugala, I., Karpinski, T. M., Goslinska-Pawlowska, O., Tulecka, T., Chudzicki, W., Szkaradkiewicz, A. K. and Zaba, R. 2012. Bacillus oleronius and Demodex mite infestation in patients with chronic blepharitis. Clin. Microbiol. Infect. 18, 1020-1025. https://doi.org/10.1111/j.1469-0691.2011.03704.x
  52. Towler, M. J. and Weathers, P. J. 2015. Variations in key artemisinic and other metabolites throughout plant development in Artemisia annua L. for potential therapeutic use. Ind. Crop. Prod. 67, 185-191. https://doi.org/10.1016/j.indcrop.2015.01.007
  53. Wang, C. Y., Ng, C. C., Su, H., Tzeng, W. S. and Shyu, Y. T. 2009. Probiotic potential of noni juice fermented with lactic acid bacteria and bifidobacteria. Int. J. Food Sci. Nutr. 60, 98-106. https://doi.org/10.1080/09637480902755095
  54. Weathers, P. J., Arsenault, P. R., Covello, P. S., McMickle, A., Teoh, K. H. and Reed, D. W. 2011. Artemisinin production in Artemisia annua: studies in planta and results of a novel delivery method for treating malaria and other neglected diseases. Phytochem. Rev. 10, 173-183. https://doi.org/10.1007/s11101-010-9166-0
  55. Wu, S. C., Su, Y. S. and Cheng, H. Y. 2011. Antioxidant properties of Lactobacillus-fermented and non-fermented Graptopetalum paraguayense E. Walther at different stages of maturity. Food Chem. 129, 804-809. https://doi.org/10.1016/j.foodchem.2011.05.025
  56. Xiao, Y., Wang, L., Rui, X., Li, W., Chen, X., Jiang, M. and Dong, M. 2015. Enhancement of the antioxidant capacity of soy whey by fermentation with Lactobacillus plantarum B1-6. J. Funct Foods 12, 33-44. https://doi.org/10.1016/j.jff.2014.10.033
  57. Xing, J., Wang, G., Zhang, Q., Liu, X., Gu, Z., Zhang, H. and Chen, W. 2015. Determining antioxidant activities of lactobacilli cell-free supernatants by cellular antioxidant assay: a comparison with traditional metthods. PloS One 10, e0119058. https://doi.org/10.1371/journal.pone.0119058