Journal of Microbiology and Biotechnology

  • 제22권7호
  • /
  • Pages.947-959
  • /
  • 2012
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Bioconversion of Isoflavones and the Probiotic Properties of the Electroporated Parent and Subsequent Three Subcultures of Lactobacillus fermentum BT 8219 in Biotin-Soymilk

  • 투고 : 2011.12.20
  • 심사 : 2012.02.24
  • 발행 : 2012.07.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

This study was aimed at an evaluation of the potential inheritance of electroporation effects on Lactobacillus fermentum BT 8219 through to three subsequent subcultures, based on their growth, isoflavone bioconversion activities, and probiotic properties, in biotin-supplemented soymilk. Electroporation was seen to cause cell death immediately after treatment, followed by higher growth than the control during fermentation in biotin-soymilk (P<0.05). This was associated with enhanced intracellular and extracellular ${\beta}$-glucosidase specific activity, leading to increased bioconversion of isoflavone glucosides to aglycones (P<0.05). The growing characteristics, enzyme, and isoflavone bioconversion activities of the first, second, and third subcultures of treated cells in biotin-soymilk were similar to the control (P>0.05). Electroporation affected the probiotic properties of parent L. fermentum BT 8219, by reducing its tolerance towards acid (pH 2) and bile, lowering its inhibitory activities against selected pathogens, and reducing its ability for adhesion, when compared with the control (P<0.05). The first, second, and third subcultures of the treated cells showed comparable traits with that of the control (P>0.05), with the exception of their bile tolerance ability, which was inherited to the treated cells of the first and second subcultures (P<0.05). Our results suggest that electroporation could be used to increase the bioactivity of biotin-soymilk via fermentation with probiotic L. fermentum BT 8219, with a view towards the development of functional foods.

키워드

참고문헌

  1. Azcarate-Peril, M. A., R. Tallon, and T. R. Klaenhammer. 2009. Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. J. Dairy Sci. 92: 870-886. https://doi.org/10.3168/jds.2008-1457
  2. Blazeka, B., J. Suskovic, and S. Matosic. 1991. Antimicrobial activity of lactobacilli and streptococci. World J. Microbiol. Biotechnol. 7: 533-536. https://doi.org/10.1007/BF00368356
  3. Bonnafous, P., M. C. Vernhes, J. Teissie, and B. Gabriel. 1999. The generation of reactive-oxygen species associated with longlasting pulse-induced electropermeabilization of mammalian cells is based on a non-destructive alteration of the plasma membrane. Biochim. Biophys. Acta 1461: 123-134. https://doi.org/10.1016/S0005-2736(99)00154-6
  4. Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  5. Chen, R. R. 2007. Permeability issues in whole-cell bioprocess and cellular membrane engineering. Appl. Microbiol. Biotechnol. 74: 730-738. https://doi.org/10.1007/s00253-006-0811-x
  6. Chun, J., J. S. Kim, and J. H. Kim. 2008. Enrichment of isoflavone aglycones in soymilk by fermentation with single and mixed cultures of Streptococcus infantarius 12 and Weissella sp. 4. Food Chem. 109: 278-284. https://doi.org/10.1016/j.foodchem.2007.12.024
  7. Coconnier, M. H., V. Lievin, M. Lorrot, and A. Servin. 2000. Antagonistic activity of Lactobacillus acidophilus LB against intracellular Salmonella enterica serovar Typhimurium infecting human enterocyte-like Caco-2/TC-7 cells. Appl. Environ. Microbiol. 66: 1152-1157. https://doi.org/10.1128/AEM.66.3.1152-1157.2000
  8. Cronan Jr, J. E. and G. L. Waldrop. 2002. Multi-subunit acetyl-CoA carboxylases. Prog. Lipid Res. 41: 407-435. https://doi.org/10.1016/S0163-7827(02)00007-3
  9. Diep, D. B., L. S. Havarstein, J. Nissen-Meyer, and I. F. Nes. 1994. The gene encoding plantaricin A, a bacteriocin from Lactobacillus plantarum C11, is located on the same transcription unit as an agr-like regulatory system. Appl. Environ. Microbiol. 60: 160-166.
  10. Elkins, C. A. and L. B. Mullis. 2004. Bile-mediated aminoglycoside sensitivity in Lactobacillus species likely results from increased membrane permeability attributable to cholic acid. Appl. Environ. Microbiol. 70: 7200-7209. https://doi.org/10.1128/AEM.70.12.7200-7209.2004
  11. Ewe, J. A., W. N. Wan-Abdullah, and M. T. Liong. 2010. Viability and growth characteristics of Lactobacillus in soymilk supplemented with B-vitamins. Int. J. Food Sci. Nutr. 61: 87-107. https://doi.org/10.3109/09637480903334163
  12. Ewe, J. A., W. N. Wan-Abdullah, B. Rajeev, A. A. Karim, and M. T. Liong. 2011. ACE inhibitory activity and bioconversion of isoflavones by Lactobacillus in soymilk supplemented with B-vitamins. Br. Food J. 113: 1127-1146. https://doi.org/10.1108/00070701111174578
  13. Ewe, J. A., W. N. Wan Abdullah, A. A. Karim, and M. T. Liong. 2012. Enhanced growth of lactobacilli and bioconversion of isoflavones in biotin-supplemented soymilk by electroporation. Int. J. Food Sci. Nutr. DOI: 10.3109/09637486.2011.641940.
  14. Forestier, C., C. De Champs, C. Vatoux, and B. Jolie. 2000. Probiotic activities of Lactobacillus casei rhamnosus: In vitro adherence to intestinal cells and antimicrobial properties. Res. Microbiol. 152: 167-173.
  15. Gajic, O., G. Buist, M. Kojic, L. Topisirovic, O. P. Kuipers, and J. Kok. 2003. Novel mechanism of bacteriocin secretion and immunity carried out by lactococcal MDR proteins. J. Biol. Chem. 278: 34291-34298. https://doi.org/10.1074/jbc.M211100200
  16. Garcia, D., P. Manas, N. Gomez, J. Raso, and R. Pagan. 2006. Biosynthetic requirements for the repair of sublethal membrane damage in Escherichia coli cells after pulsed electric fields. J. Appl. Microbiol. 100: 428-435. https://doi.org/10.1111/j.1365-2672.2005.02795.x
  17. Gaudreau, H., C. P. Champagne, and P. Jelen. 2005. The use of crude cellular extracts of Lactobacillus delbrueckii spp. bulgaricus 11842 to stimulate growth of a probiotic Lactobacillus rhamnosus culture in milk. Enzyme Microb. Technol. 36: 83-90. https://doi.org/10.1016/j.enzmictec.2004.06.006
  18. Golowczyc, M. A., J. Silva, P. Teixeira, G. L. De Antoni, and A. G. Abraham. 2011. Cellular injuries of spray-dried Lactobacillus spp. isolated from kefir and their impact on probiotic properties. Int. J. Food Microbiol. 144: 556-560. https://doi.org/10.1016/j.ijfoodmicro.2010.11.005
  19. Golzio, M., M. P. Rols, and J. Teissie. 2004. In vitro and in vivo electric field-mediated permeabilization, gene transfer, and expression. Methods 33: 126-135. https://doi.org/10.1016/j.ymeth.2003.11.003
  20. Holo, H., Z. Jeknic, M. Daeschel, S. Stevanovic, and I. F. Nes. 2001. Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology 147: 643-651
  21. Hong, S. I., Y. J. Kim, and Y. R. Pyun. 1999. Acid tolerance of Lactobacillus plantarum from kimchi. Lebensm. Wiss. Technol. 32: 142-148. https://doi.org/10.1006/fstl.1998.0517
  22. Jimenez-Diaz, R., R. M. Rioz-Sanchez, M. Desmazeaud, J. L. Ruiz-Barba, and J. C. Piard. 1993. Plantaricins S and T, two new bacteriocins produced by Lactobacillus plantarum LPCO10 isolated from a green olive fermentation. Appl. Environ. Microbiol. 59: 1416-1424.
  23. Jimenez-Diaz, R., J. L. Ruiz-Barba, D. P. Cathcart, H. Holo, I. F. Nes, K. H. Sletten, and P. J. Warner. 1995. Purification and partial amino acid sequence of plantaricin S, a bacteriocin produced by Lactobacillus plantarum LPCO10, the activity of which depends on the complementary action of two peptides. Appl. Environ. Microbiol. 61: 4459-4463.
  24. Kanduser, M., M. Sentjurc, and D. Miklavcic. 2006. Cell membrane fluidity related to electroporation and resealing. Eur. Biophys. J. 35: 196-204. https://doi.org/10.1007/s00249-005-0021-y
  25. Kano, M., T. Takayanagi, K. Harada, S. Sawada, and F. Ishikawa. 2006. Bioavailability of isoflavones after ingestion of soy beverages in healthy adults. J. Nutr. 136: 2291-2296.
  26. Kimoto, H., S. Ohmomo, and T. Okamoto. 2002. Enhancement of bile tolerance in lactococci by Tween 80. J. Appl. Microbiol. 92: 41-46. https://doi.org/10.1046/j.1365-2672.2002.01505.x
  27. Kirjavainen, P. V., A. C. Ouwehand, E. Isolauri, and S. J. Salminen. 1998. The ability of probiotic bacteria to bind to human intestinal mucus. FEMS Microbiol. Lett. 67: 185-189.
  28. Leontiadou, H., A. E. Mark, and S. J. Marrink. 2004. Molecular dynamics simulations of hydrophilic pores in lipid bilayers. Biophys. J. 86: 2156-2164. https://doi.org/10.1016/S0006-3495(04)74275-7
  29. Lievin-Le Moal, V., R. Amsellem, A. L. Servin, and M. H. Coconnier. 2002. Lactobacillus acidophilus (strain LB) from resident human adult gastrointestinal microflora exerts activity against brush border damage promoted by a diarrhoeagenic Escherichia coli in human enterocyte-like cells. Gut 50: 803-811. https://doi.org/10.1136/gut.50.6.803
  30. Loghavi, L., S. K. Sastry, and A. E. Yousef. 2007. Effect of moderate electric field on the metabolic activity and growth kinetics of Lactobacillus acidophilus. Biotechnol. Bioeng. 98: 872-881. https://doi.org/10.1002/bit.21465
  31. Mahajan, P. M., K. M. Desai, and S. S. Lele. 2010. Production of cell membrane-bound ${\alpha}$-and ${\beta}$-glucosidase by Lactobacillus acidophilus. Food Bioprocess Technol. 5: 706-718.
  32. Martin, R., S. Delgado, A. Maldonado, E. Jimenez, M. Olivares, L. Fernandez, O. J. Sobrino, and J. M. Rodriguez. 2009. Isolation of lactobacilli from sow milk and evaluation of their probiotic potential. J. Dairy Res. 76: 418-425. https://doi.org/10.1017/S0022029909990124
  33. Murga, M. L. F., D. Bernik, G. F. de Valdez, and A. E. Disalvo. 1999. Permeability and stability properties of membranes formed by lipids extracted from Lactobacillus acidophilus grown at different temperatures. Arch. Biochem. Biophys. 364: 115-121. https://doi.org/10.1006/abbi.1998.1093
  34. Ohshima, T. and M. Sato. 2004. Extracellular release of recombinant ${\alpha}-amylase$ from Escherichia coli using pulsed electric field. Biotechnol. Progr. 20: 1528-1533. https://doi.org/10.1021/bp049760u
  35. Ouwehand, A. C., P. V. Kirjavainen, M. M. Gronlund, E. Isolauri, and S. J. Salminen. 1999. Adhesion of probiotic microorganisms to intestinal mucus. Int. Dairy J. 9: 623-630. https://doi.org/10.1016/S0958-6946(99)00132-6
  36. Perni, S., P. R. Chalise, G. Shama, and M. G. Kong. 2007. Bacterial cells exposed to nanosecond pulsed electric fields show lethal and sublethal effects. Int. J. Food Microbiol. 120: 311-314. https://doi.org/10.1016/j.ijfoodmicro.2007.10.002
  37. Prado-Acosta, M., S. M. Ruzal, M. C. Allievi, M. M. Palomino, and R. C. Sanchez. 2009. Synergistic effects of the Lactobacillus acidophilus S-layer and nisin on bacterial growth. Appl. Environ. Microbiol. 116: 405-409.
  38. Prasanna, G. L. and T. Panda. 1997. Electroporation: Basic principles, practical considerations and applications in molecular biology. Bioprocess Biosyst. Eng. 16: 164-261.
  39. Raso, J. and V. Heinz. 2006. Pulsed Electric Fields Technology for the Food Industry. Food Engineering Series. Springer Verlag, Heidelberg.
  40. Rols, M. P. 2006. Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells. Biochim. Biophys. Acta 1758: 423-428. https://doi.org/10.1016/j.bbamem.2006.01.005
  41. Schar-Zammaretti, P. and J. Ubbink. 2003. The cell wall of lactic acid bacteria: Surface and macromolecular conformations. Biophys. J. 85: 4076-4092. https://doi.org/10.1016/S0006-3495(03)74820-6
  42. Schillinger, U., C. Guigas, and W. H. Holzapfel. 2005. In vitro adherence and other properties of lactobacilli used in probiotic yogurt-like products. Int. Dairy J. 15: 1289-1297. https://doi.org/10.1016/j.idairyj.2004.12.008
  43. Servin, A. L. and M. H. Coconnier. 2003. Adhesion of probiotic strains to the intestinal mucosa and the interaction with pathogens. Best Pract. Res. Clin. Gastroenterol. 17: 741-754. https://doi.org/10.1016/S1521-6918(03)00052-0
  44. Setchell, K. D. R., N. M. Brown, L. Zimmer-Nechemias, W. T. Brasheas, B. E. Wolfe, A. S. Krischner, and J. E. Heubi. 2002. Evidence for the lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Am. J. Clin. Nutr. 76: 447-453.
  45. Shariff, M. Z. 2008. Utilization of transient electroporation in intensified bioprocessing: A study for the enhancement of Lglutamate production by corynebacteria. PhD Thesis. Department of Chemical Engineering, School of Engineering and Physical Sciences, Heriot Watt University, Edinburgh, UK.
  46. Silva, M., N. V. Jacobus, C. Deneke, and S. L. Gorbach. 1987. Antimicrobial substance from a human Lactobacillus strain. Antimicrob. Agents Chemother. 31: 1231-1233. https://doi.org/10.1128/AAC.31.8.1231
  47. Teh, S. S., R. Ahmad, W. N. Wan Abdullah, and M. T. Liong. 2009. Evaluation of agrowastes as immobilizers for probiotics in soymilk. J. Agric. Food Chem. 57: 10187-10198. https://doi.org/10.1021/jf902003a
  48. Teissie, J., N. Eynard, B. Gabriel, and M. P. Rols. 1999. Electropermeabilization of cell membranes. Adv. Drug Deliv. Rev. 35: 3-19. https://doi.org/10.1016/S0169-409X(98)00060-X
  49. Tryfona, T. and M. T. Bustard. 2008. Impact of pulsed electric fields on Corynebacterium glutamicum cell membrane permeabilization. J. Biosci. Bioeng. 105: 375-382. https://doi.org/10.1263/jbb.105.375
  50. Vaughan, E. E., B. Mollet, and W. M. Devos. 1999. Functionality of probiotics and intestinal lactobacilli: Light in the intestinal tract tunnel. Curr. Opin. Biotechnol. 10: 505-510. https://doi.org/10.1016/S0958-1669(99)00018-X
  51. Weaver, J. C. 2000. Electroporation of cells and tissues. IEEE Transac. Plasma Sci. 28: 24-33. https://doi.org/10.1109/27.842820
  52. Wei, Q.-K., T.-R. Chen, and J.-T. Chen. 2007. Using of Lactobacillus and Bifidobacterium to product the isoflavone aglycones in fermented soymilk. Int. J. Food Microbiol. 117: 120-124. https://doi.org/10.1016/j.ijfoodmicro.2007.02.024
  53. Wouters, P. C., A. P. Bos, and J. Ueckert. 2001. Membrane permeabilization in relation to inactivation kinetics of Lactobacillus species due to pulsed electric fields. Appl. Environ. Microbiol. 67: 3092-3101. https://doi.org/10.1128/AEM.67.7.3092-3101.2001
  54. Xu, G. Q., J. Chu, Y. P. Zhuang, Y. H. Wang, and S. L. Zhang. 2008. Effects of vitamins on the lactic acid biosynthesis of Lactobacillus paracasei NERCB 0401. Biochem. Eng. J. 38: 189-197. https://doi.org/10.1016/j.bej.2007.07.003
  55. Yeo, S. K. and M. T. Liong. 2010. Angiotensin I-converting enzyme inhibitory activity and bioconversion of isoflavones by probiotics in soymilk supplemented with prebiotics. Int. J. Food Sci. Nutr. 61: 161-181. https://doi.org/10.3109/09637480903348122
  56. Yokota, A., M. Veenstra, P. Kurdi, H. W. van Veen, and W. N. Konings. 2000. Cholate resistance in Lactococcus lactis is mediated by an ATP-dependent multispecific organic anion transporter. J. Bacteriol. 182: 5196-5201. https://doi.org/10.1128/JB.182.18.5196-5201.2000

피인용 문헌

  1. Fermentation at non-conventional conditions in food- and bio-sciences by the application of advanced processing technologies vol.38, pp.1, 2018, https://doi.org/10.1080/07388551.2017.1312272
  2. Bioconversion of γ-aminobutyric acid and isoflavone contents during the fermentation of high-protein soy powder yogurt with Lactobacillus brevis vol.61, pp.4, 2018, https://doi.org/10.1007/s13765-018-0366-4
  3. Change in physicochemical properties, phytoestrogen content, and antioxidant activity during lactic acid fermentation of soy powder milk obtained from colored small soybean vol.25, pp.6, 2012, https://doi.org/10.11002/kjfp.2018.25.6.696
  4. Recent insights in the impact of emerging technologies on lactic acid bacteria: A review vol.137, pp.None, 2012, https://doi.org/10.1016/j.foodres.2020.109544