Korean Journal of Microbiology (미생물학회지)

The Microbiological Society of Korea (한국미생물학회)
권호 표지
DOI QR코드

DOI QR Code

Optimal conditions and effects of prebiotics for growth and antimicrobial substances production of Lactobacillus brevis BK11

Lactobacillus brevis BK11의 증식과 항균물질 생산을 위한 최적 배양조건 및 prebiotics의 영향

  • Lim, Eun-Seo (Department of Food Science and Nutrition, Tongmyong University)
  • 임은서 (동명대학교 식품영양학과)
  • Received : 2015.08.20
  • Accepted : 2015.09.23
  • Published : 2015.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Lactobacillus brevis BK11 obtained from Baikkimchi was selected to study the effects of culture medium, initial pH, atmosphere composition, incubation temperature and time, and prebiotics on growth and production of antimicrobial substances. Growth and antimicrobial substances production of L. brevis BK11 were significantly higher in MRS broth than in BHI or M17 broth. The production of cell mass, lactic acid, and bacteriocin by BK11 strain was at maximum in MRS broth adjusted to pH 6.0. Aerobic and microaerobic conditions were favored cell growth and antimicrobial substances production than anaerobic condition. Biomass and lactic acid production and antimicrobial substances activity of BK 11 were significantly better at 30 and $37^{\circ}C$ than at $25^{\circ}C$. Growth of the strain BK11 entered the stationary growth stage at 24 h after inoculation, and decreased after 36 h. Antimicrobial activities of cell-free culture supernatant and bacteriocin solution were highest when cultured in MRS broth with an initial pH 6.0 for 24-30 h at $37^{\circ}C$. In addition, the highest cell number and lactic acid and bacteriocin production were recorded in the presence of 1 and 2% (w/v) fructooligosaccharide (FOS), however, inulin and raffinose did not affect biological and physicochemical characteristics and antimicrobial activities of L. brevis BK11 cultures. According to these results, production of antimicrobial substances by L. brevis KB11 was closely associated with cell density. Under optimal conditions for antimicrobial substances production, L. brevis BK11 effectively inhibited the growth of Helicobacter pylori ATCC 43504.

숙성된 백김치로부터 얻은 Lactobacillus brevis BK11의 증식과 항균물질 생산에 대한 배양용 배지 종류, 공기 조성, 초기 pH, 배양온도 및 시간과 프리바이오틱스의 영향을 조사하였다. L. brevis BK11의 증식과 항균물질 활성은 BHI와 M17 배지 보다는 MRS 배지 상에서 더 높게 나타났으며, 배지의 초기 pH 6.0에서 생산량이 최대에 이르렀다. 혐기적 조건보다는 호기적 및 미호기적 조건에서 배양했을 때와 $25^{\circ}C$ 보다는 $30^{\circ}C$와 $37^{\circ}C$ 온도에서 배양했을 때 균 성장과 항균물질 생산에 유리하였다. BK11 균주는 배양 24시간 만에 정지기에 도달하였고, 36시간 후부터는 생균수가 감소되었고, 배양상등액과 박테리오신 용액의 항균 활성은 $37^{\circ}C$, 24-30시간 배양했을 때 가장 높았다. 세포수와 유산 및 박테리오신 생산은 프락토올리고당 1-2% 첨가한 경우에 가장 높았으나, 이뉼린과 라피노오스는 균 증식에 별다른 도움을 주지 못했다. 결과적으로 L. brevis BK11의 항균물질 생산은 세포수와 관계 있었으며, 이러한 최적 조건 하에서 배양한 경우 Helicobacter pylori ATCC 43504의 성장을 효과적으로 저해할 수 있다.

Keywords

References

  1. Aiba, Y., Suzuki, N., Kabir, A.M., Takagi, A., and Koga, Y. 1998. Lactic acid-mediated suppression of Helicobacter pylori of Lactobacillus salivarius as a probiotic in gnotobiotic murine model. Am. J. Gastroenterol. 93, 2097-2101. https://doi.org/10.1111/j.1572-0241.1998.00600.x
  2. Al-Jumaily, E., Raheema, R.H., and Abdul-Ratha, H.A. 2014. Optimal conditions for acidocin production from Lactobacillus acidophilus isolate. World J. Pharm. Res. 3, 1773-1785.
  3. Aslam, M., Shahid, M., Ur Rehman, F., Murtaza, M.A., Sharif, S., Ata, A., and Noor, S. 2012. Production optimization and characterization of a low molecular weight bacteriocin from Lactococcus lactis subsp. lactis. Afr. J. Microbiol. Res. 6, 5924-5933.
  4. Audisio, M.C., Oliver, G., and Apella, M.C. 2001. Effect of different complex carbon sources on growth and bacteriocin synthesis of Enterococcus faecium. Int. J. Food Microbiol. 63, 235-241. https://doi.org/10.1016/S0168-1605(00)00429-3
  5. Biswas, S.R., Ray, P., Johnson, M.C., and Ray, B. 1991. Influence of growth conditions on the production of a bacteriocin, pediocin AcH, by Pediococcus acidilactici H. Appl. Environ. Microbiol. 57, 1265-1267.
  6. Cabo, M.L., Murado, M.A., Gonza'lez, M.P., and Pastoriza, L. 2001. Effects of aeration and pH gradient on nisin production. A mathematical model. Enzyme Microb. Tech. 29, 264-273. https://doi.org/10.1016/S0141-0229(01)00378-7
  7. Chen, X., Liu, X.M., Tian, F., Zhang, Q., Zhang, H.P., Zhang, H., and Chen, W. 2011. Antagonistic activities of lactobacilli against Helicobacter pylori growth and infection in human gastric epithelial cells. J. Food Sci. 71, M9-M14.
  8. Chen, Y.S., Srionnual, S., Onda, T., and Yanagida, F. 2007. Effects of prebiotic oligosaccharides and trehalose on growth and production of bacteriocins by lactic acid bacteria. Lett. Appl. Microbiol. 45, 190-193. https://doi.org/10.1111/j.1472-765X.2007.02167.x
  9. Chin, H.S., Shim, J.S., Kim, J.M., Yang, R., and Yoon, S.S. 2001. Detection and antibacterial activity of a bacteriocin produced by Lactobacillus plantarum. Food Sci. Biotechnol. 10, 461-467.
  10. Cho, H.Y., Yousef, A.E., and Yang, S.T. 1996. Continuous production of pediocin by immobilized Pediococcus acidilactici PO2 in a packed-bed bioreactor. Appl. Microbiol. Biotechnol. 45, 589-594. https://doi.org/10.1007/s002530050734
  11. Coconnier, M.H., Lievin, V., Hemery, E., and Servin, A.L. 1998. Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl. Environ. Microbiol. 64, 4573-4580.
  12. Crittenden, R.G. 1999. Prebiotics, Probiotics: A Critical Review, pp. 141-156. In Tannock, G.W. (ed.), Horizon Scientific Press, Wymondham.
  13. Daba, H., Pandian, S., Gosselin, J.F., Simard, R.E., Huang, J., and Lacroix, C. 1993. Detection and activity of a bacteriocin by Leuconostoc mesenteroides. Appl. Environ. Microbiol. 57, 3450-3455.
  14. De Lima, C.J.B., Coelho, L.F., and Contiero, J. 2010. The use of response surface methodology in optimization of lactic acid production: Focus on medium supplementation, temperature and pH control. Food Technol. Biotechnol. 48, 175-181.
  15. De Vuyst, L. and Vandamme, E.J. 1992. Influence of the phosphorus and nitrogen source of nisin production in Lactococcus lactis subsp. lactis batch fermentations using a complex medium. Appl. Microbiol. Biotechnol. 40, 17-22.
  16. De Vuyst, L. and Vandamme, E.J. 1993. Influence of the phosphorus and nitrogen source on nisin production in Lactococcus lactis subsp. lactis batch fermentations using a complex medium. Appl. Microbiol. Biotechnol. 40, 17-22. https://doi.org/10.1007/BF00170422
  17. Deegan, L.H., Cotter, P.D., Hill, C., and Ross, P. 2006. Bacteriocins:Biological tools for bio-preservation and shelf-life extension. Int. Dairy J. 16, 1058-1071. https://doi.org/10.1016/j.idairyj.2005.10.026
  18. Devriese, L.A., Pot, B., and Collins, M.D. 1993. A review. Phenotypic identification of the genus Enterococcus and differentiation of phylogenetically distinct enterococcal species and species group. J. Appl. Bacteriol. 75, 399-408. https://doi.org/10.1111/j.1365-2672.1993.tb02794.x
  19. Egan, B.J., Katicic, M., O'connor, H.J., and O'Morain, C.A. 2007. Treatment of Helicobacter pylori. Helicobacter 12, 31-37. https://doi.org/10.1111/j.1523-5378.2007.00538.x
  20. Farinha, L.L., Sabo, S.S., Porto, M.C., Souza, E.C., Oliveira, M.N., and Oliveira, R.P.S. 2015. Influence of prebiotic ingredients on the growth kinetics and bacteriocin production of Lactococcus lactis. Chem. Eng. 43, 313-318.
  21. Fukushima, H., Kelstrup, J., Fukushima, S., Umemoto T., and Sagawa, H. 1983. Isolation, partial purification and preliminary characterization of a bacteriocin from Streptococcus mutants Rm-10. Antonie van Leeuwenhoek 49, 41-50. https://doi.org/10.1007/BF00457878
  22. 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
  23. Gibson, G.R. and Roberfroid, M.B. 1995. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 125, 1401-1412.
  24. Goderska, K., Nowak, J., and Czarnecki, Z. 2008. Comparison of the growth of Lactobacillus acidophilus and Bifidobacterium bifidium species in media supplemented with selected saccharides including prebiotics. Acta. Sci. Pol. Tehcnol. Aliment. 7, 5-20.
  25. Gotteland, M., Brunser, O., and Cruchet S. 2006. Systematic review:Are probiotics useful in controlling gastric colonization by Helicobacter pylori? Aliment Pharmacol. Ther. 23, 1077-1086. https://doi.org/10.1111/j.1365-2036.2006.02868.x
  26. Guerra, N.P., Rua, M.L., and Pastrana, L. 2001. Nutritional factors affecting the production of two bacteriocins from lactic acid bacteria on whey. Int. J. Food Microbiol. 70, 267-281. https://doi.org/10.1016/S0168-1605(01)00551-7
  27. Hirsch, A. 1951. Grwoth and nisin production of a strain of Streptococcus lactis. J. Gen. Microbiol. 5, 208-221. https://doi.org/10.1099/00221287-5-1-208
  28. Hole, H., Nilssen, O., and Nes, I.F. 1991. Lactococcin A, a new bacteriocin from Lactococcus lactis subsp. cremoris: Isolation and characterization of the protein and its gene. J. Bacteriol. 173, 3879-3887. https://doi.org/10.1128/jb.173.12.3879-3887.1991
  29. Joosten, H.M.L.J. and Nunez, M. 1995. Adsorption of nisin and enterocin 4 to polypropylene and glass surface and its prevention by Tween 80. Lett. Appl. Microbiol. 21, 389-392. https://doi.org/10.1111/j.1472-765X.1995.tb01089.x
  30. Jozala, A.F., De Andrade, M.S., De Arauz, L.J., Pessoa, A.J., and Penna, T.C. 2007. Nisin production utilizing skimmed milk aiming to reduce process cost. Appl. Biochem. Biotechnol. 137, 515-528.
  31. Juarez Tomas, M.S., Bru, E., Wiese, B., De Ruiz Holgado, A.A.P., and Nader-Macias, M.E. 2002. Influence of pH, temperature and culture media on the growth and bacteriocin production by vaginal Lactobacillus salivarius CRL 1328. J. Appl. Microbiol. 93, 714-724. https://doi.org/10.1046/j.1365-2672.2002.01753.x
  32. Juarez Tomas, M.S., Ocana, V.S., Wiese, B., and Nader-Macias, M.E. 2003. Growth and lactic acid production by vaginal Lactobacillus acidophilus CRL 1259, and inhibition of uropathogenic Escherichia coli. J. Med. Microbiol. 52, 1117-1124. https://doi.org/10.1099/jmm.0.05155-0
  33. Kim, W.S., Hall, R.J., and Dunn, N.W. 1997. The effect of nisin concentration and nutrient depletion on nisin production of Lactococcus lactis. Appl. Microbiol. Biotechnol. 136, 1591-1599.
  34. Kim, T.S., Hur, J.W., Yu, M.A., Cheigh, C.I., Kim, K.N., Hwang, J.K., and Pyun, Y.R. 2003. Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J. Food Prot. 66, 3-12. https://doi.org/10.4315/0362-028X-66.1.3
  35. Kondepudi, K.K., Ambalam, P., Nilsson, I., Wadstrom, W., and Ljungh, A. 2012. Prebiotic-digestible oligosaccharides preference of probiotic bifidobacteria and antimicrobioal activity against Clostridium difficile. Anaerobe 18, 489-497. https://doi.org/10.1016/j.anaerobe.2012.08.005
  36. Kusters, J.G., Van Vliet, A.H.M., and Kuipers, E.J. 2006. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 19, 449-490. https://doi.org/10.1128/CMR.00054-05
  37. Lee, N.K., Kim, K.T., Kim, C.J., and Paik, H.D. 2004. Optimized production of lacticin NK24, a bacteriocin produced by Lactococcus lactis NK24 isolated from Jeot-gal. Food Sci. Biotechnol. 13, 6-10.
  38. Leroy, F. and De Vuyst, L. 1999. Temperature and pH conditions that prevail during fermentation of sausages are optimal for production of the antilisterial bacteriocin sakacin K. Appl. Environ. Microbiol. 65, 974-981.
  39. Leroy, F., Vankrunkelsven, S., De Greef, J., and De Vuyst, L. 2003. The stimulating effect of a harsh environment on the bacteriocin activity by Enterococcus faecium RZS C5 and dependency on the environmental stress factor used. Int. J. Food Microbiol. 83, 27-38. https://doi.org/10.1016/S0168-1605(02)00316-1
  40. Lesbros-Pantoflickova, D., Corthesy-Theulaz, I., and Blum, A.L. 2007. Helicobacter pylori and probiotics. J. Nutr. 137, 812S-818S. https://doi.org/10.1093/jn/137.3.812S
  41. Lim, S.M. 2014. Anti-Helicobacter pylori activity of antimicrobial substances produced by lactic acid bacteria isolated from baikkimchi. J. Kor. Soc. Appl. Biol. Chem. 57, 621-630. https://doi.org/10.1007/s13765-014-4198-6
  42. Mahrous, H., Mohamed, A., El-Mongy, A., El-Batal, A.I., and Hamza, H.A. 2013. Study bacteriocin production and optimization using new isolates of Lactobacillus spp. isolated from some dairy products under different culture conditions. Food Nutr. Sci. 4, 342-356. https://doi.org/10.4236/fns.2013.43045
  43. Makelainen, H., Saarien, M., Stowell, J., Rautonen, N., and Ouwehand, A.C. 2010. Xylo-oligosaccharides and lactitol promote the growth of Bifidobacterium lactis and Lactobacillus species in pure cultures. Benef. Microbes 1, 139-148. https://doi.org/10.3920/BM2009.0029
  44. Marshall, B.J. and Warren, J.R. 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1, 1311-1315.
  45. Matsusaki, H., Endo, N., Sonomoto, K., and Ishikazi, A. 1996. Lantibiotics nisin Z fermentative production by Lactococcus lactis IO-1: relationship between production of the lantibiotic and lactate and cell growth. Appl. Microbiol. Biotechnol. 45, 36-40. https://doi.org/10.1007/s002530050645
  46. Megraud, F., Coenen, S., Versporten, A., Kist, M., Lopez-Brea, M., Hirsch, A.M., Andersen, L.P., Goossens, H., and Glupczynski, Y. 2013. Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut 62, 34-42. https://doi.org/10.1136/gutjnl-2012-302254
  47. Mitra, S., Chakrabartty, P.K., and Biswas, S.R. 2007. Production of nisin A by Lactococcus lactis isolated from Dahi. Appl. Biochem. Biotechnol. 143, 41-53. https://doi.org/10.1007/s12010-007-0032-5
  48. Munoz, M., Mosquera, A., Almeciga-Diaz, C.J., Melendez, A.P., and Sanchez, O.F. 2012. Fructooligosaccharides metabolism and effect on bacteriocin production in Lactobacillus strains isolated from ensiled corn and molasses. Anaerobe 18, 321-330. https://doi.org/10.1016/j.anaerobe.2012.01.007
  49. Nam, H., Ha, M., Bae, O., and Lee, Y. 2002. Effect of Weissella confuse strain PL9001 on the adherence and growth of Helicobacter pylori. Appl. Environ. Microbiol. 68, 4642-4645. https://doi.org/10.1128/AEM.68.9.4642-4645.2002
  50. Ogunbanwo, S.T., Sanni, A.I., and Onilude, A.A. 2003. Influence of cultural conditions on the production of bacteriocin by Lactobacillus brevis OG1. Afr. J. Biotechnol. 2, 179-184. https://doi.org/10.5897/AJB2003.000-1037
  51. Parente, E. and Ricciardi, A. 1999. Production, recovery and purification of bacteriocins from lactic acid bacteria. Appl. Microbiol. Biotechnol. 52, 628-638. https://doi.org/10.1007/s002530051570
  52. Rattanachaikunsopon, P. and Phumkhachorn, P. 2010. Lactic acid bacteria: their antimicrobial compounds and their uses in food production. Ann. Biol. Res. 1, 218-228.
  53. Sgouras, D., Maragkoudakis, P., Petraki, K., Martinez-Gonzalez, B., Eriotou, E., Michopoulos, S., Kalantzopoulos, G., Tsakalidou, E., and Mentis, A. 2004. In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strain Shirota. Appl. Environ. Microbiol. 70, 518-526. https://doi.org/10.1128/AEM.70.1.518-526.2004
  54. Sousa, M.N.B., Mendes, E.N., Apolonio, A.C.M., Farias, L.D.M., and Magalha, E.S. 2010. Bacteriocin production by Shigella sonnei isolated from faeces of children with acute diarrhea. APMIS 118, 125-135. https://doi.org/10.1111/j.1600-0463.2009.02570.x
  55. Taheri, P., Samadi, N., Ehsani, M.R., Khoshayand, M.R., and Jamalifar, H. 2012. An evaluation and partial characterization of a bacteriocin produced by Latococcus lactis subsp. lactis ST1 isolated from goat milk. Braz. J. Microbiol. 43, 1452-1462. https://doi.org/10.1590/S1517-83822012000400029
  56. Tongtawee, T., Dechsukhum, C., Leeanansaksiri, W., Kaewpitoon, S., Kaewpitoon, N., Loyd, R.A., Matrakool, L., and Panpimanmas, S. 2015. Effect of pretreatment with Lactobacillus delbrueckii and Streptococcus thermophillus on tailored triple therapy for Helicobacter pylori eradication: A prospective randomized controlled clinical trial. Asian Pac. J. Cancer Prev. 16, 4885-4890. https://doi.org/10.7314/APJCP.2015.16.12.4885
  57. Tsai, C.C., Huang, L.F., Lin, C.C., and Tsen, H.Y. 2004. Antagonistic activity against Helicobacter pylori infection in vitro by a strain of Enterococcus faecium TM39. Int. F. Food Microbiol. 96, 1-12. https://doi.org/10.1016/j.ijfoodmicro.2003.10.019
  58. Vakil, N. and Megraud, F. 2007. Eradication therapy for Helicobacter pylori. Gastroenterology 133, 985-1001. https://doi.org/10.1053/j.gastro.2007.07.008
  59. Verellen, T.L.J., Bruggeman, G., Van Reenen, C.A., Dicks, L.M.T., and Vandamme, E.J. 1998. Fermentation optimization of plantaricin 423, a bacteriocin produced by Lactobacillus plantarum 423. J. Ferment. Bioeng. 86, 147-179.
  60. Vitor, J.M. and Vale, F.F. 2011. Alternative therapies for Helicobacter pylori: probiotics and phytomedicine. FEMS Immunol. Med. Microbiol. 63, 153-164. https://doi.org/10.1111/j.1574-695X.2011.00865.x
  61. Wee, Y.J., Kim, J.N., Yun, J.S., and Ryu, H.W. 2005. Optimum conditions for the biological production of lactic acid by a newly isolated lactic acid bacterium, Lactobacillus sp. RKY2. Biotechnol. Bioprocess Eng. 10, 23-28. https://doi.org/10.1007/BF02931178
  62. Yoo, I.K., Chang, H.N., Lee, E.G., Chang, Y.K., and Moon, S.H. 1996. Effect of pH on the production of lactic acid and secondary products in batch cultures of Lactobacillus casei. J. Microbiol. Biotechnol. 6, 482-486.
  63. Yoo, J.Y., Lee, I.S., Chung, K.S., Choi, S.Y., Koo, Y.J., and Kwon, D.J. 1992. Cultural conditions of Lactococcus sp. 112-1 for production of bacteriocin-like substance. Kor. J. Appl. Microbiol. Biotechnol. 20, 183-189.

Cited by

  1. Bacillus subtilis KCCM 11965P를 이용한 붉은팥 발효물의 항산화 활성 및 이화학성분 분석 vol.24, pp.7, 2017, https://doi.org/10.11002/kjfp.2017.24.7.975
  2. 프로바이오틱 Lactobacillus brevis SBB07의 균체량 증가를 위한 배양 조건 최적화 vol.28, pp.5, 2018, https://doi.org/10.5352/jls.2018.28.5.577
  3. Preparation of Carbon Source for Modified MRS Medium and Antibacterial Activity of Bacteriocin from L. plantarum vol.23, pp.1, 2015, https://doi.org/10.13050/foodengprog.2019.23.1.47