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http://dx.doi.org/10.4014/jmb.1112.12044

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

Ewe, Joo-Ann (School of Industrial Technology, Universiti Sains Malaysia)
Wan-Abdullah, Wan-Nadiah (School of Industrial Technology, Universiti Sains Malaysia)
Alias, Abdul Karim (School of Industrial Technology, Universiti Sains Malaysia)
Liong, Min-Tze (School of Industrial Technology, Universiti Sains Malaysia)
Publication Information
Journal of Microbiology and Biotechnology / v.22, no.7, 2012 , pp. 947-959 More about this Journal
Abstract
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.
Keywords
Electroporation; Lactobacillus fermentum; biotin-soymilk; isoflavones; probiotic properties; subcultures;
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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.   DOI   ScienceOn
2 Blazeka, B., J. Suskovic, and S. Matosic. 1991. Antimicrobial activity of lactobacilli and streptococci. World J. Microbiol. Biotechnol. 7: 533-536.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
5 Chen, R. R. 2007. Permeability issues in whole-cell bioprocess and cellular membrane engineering. Appl. Microbiol. Biotechnol. 74: 730-738.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
8 Cronan Jr, J. E. and G. L. Waldrop. 2002. Multi-subunit acetyl-CoA carboxylases. Prog. Lipid Res. 41: 407-435.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
13 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.   DOI   ScienceOn
14 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.
15 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.
16 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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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 Kanduser, M., M. Sentjurc, and D. Miklavcic. 2006. Cell membrane fluidity related to electroporation and resealing. Eur. Biophys. J. 35: 196-204.   DOI
22 Hong, S. I., Y. J. Kim, and Y. R. Pyun. 1999. Acid tolerance of Lactobacillus plantarum from kimchi. Lebensm. Wiss. Technol. 32: 142-148.   DOI   ScienceOn
23 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.
24 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.
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.   DOI   ScienceOn
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.   DOI   ScienceOn
29 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.   DOI   ScienceOn
30 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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
37 Rols, M. P. 2006. Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells. Biochim. Biophys. Acta 1758: 423-428.   DOI   ScienceOn
38 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.
39 Prasanna, G. L. and T. Panda. 1997. Electroporation: Basic principles, practical considerations and applications in molecular biology. Bioprocess Biosyst. Eng. 16: 164-261.
40 Raso, J. and V. Heinz. 2006. Pulsed Electric Fields Technology for the Food Industry. Food Engineering Series. Springer Verlag, Heidelberg.
41 Schar-Zammaretti, P. and J. Ubbink. 2003. The cell wall of lactic acid bacteria: Surface and macromolecular conformations. Biophys. J. 85: 4076-4092.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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 Tryfona, T. and M. T. Bustard. 2008. Impact of pulsed electric fields on Corynebacterium glutamicum cell membrane permeabilization. J. Biosci. Bioeng. 105: 375-382.   DOI   ScienceOn
47 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.   DOI   ScienceOn
48 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.   DOI   ScienceOn
49 Teissie, J., N. Eynard, B. Gabriel, and M. P. Rols. 1999. Electropermeabilization of cell membranes. Adv. Drug Deliv. Rev. 35: 3-19.   DOI   ScienceOn
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.   DOI   ScienceOn
51 Weaver, J. C. 2000. Electroporation of cells and tissues. IEEE Transac. Plasma Sci. 28: 24-33.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
55 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.   DOI   ScienceOn
56 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.   DOI   ScienceOn