Abstract
The aim of our study was to evaluate the potential ramifications of sub-lethal ultraviolet B radiation (SUVBR) on Lactobacillus fermentum BT 8219 cells through to three subsequent subcultures during fermentation in biotin-supplemented soymilk (biotin-soymilk). Lactobacillus fermentum BT 8219 cultures were irradiated in Petri dishes (diameter 56 cm2) with UVB at a dosage of 60 J m−2 using a GS Gene Linker UV Chamber. Cell lethality was observed immediately after SUVBR, followed by higher growth than that shown by the control during fermentation in biotin-soymilk (P < 0.05). This enhanced growth was associated with enhanced β-glucosidase specific activity, leading to increased bioconversion of isoflavone glucosides to aglycones (P < 0.05). The first, second and third subcultures of the treated cells and the control showed similar growing characteristics, enzymes and isoflavone bioconversion activities in biotin-soymilk (P > 0.05). In comparison to the control, SUVBR affected the functional properties of parent cells by reducing their tolerability towards acid (pH 2) and bile, lowering their inhibitory activities against selected pathogens and reducing their ability for adhesion (P < 0.05). Acid tolerance and adhesion ability of the subsequent subcultures of the treated cells showed comparable traits with the control (P> 0.05), while reduced bile tolerance and antimicrobial property were observed up to the second subcultures of the treated cells (P < 0.05). Our results suggest that SUVBR could be utilised to produce putative probiotic cells and to increase the bioactivity of biotin-soymilk via fermentation with L. fermentum BT 8219 for the development of functional foods.
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References
Azcarate-Peril MA, Tallon R, Klaenhammer TR (2009) Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. J Dairy Sci 92:870–886
Baumstark-Khan C, Hentschel U, Nikandrova Y, Krug J, Horneck G (2000) Fluorometric analysis of DNA unwinding (FADU) as a method for detecting repair-induced DNA strand breaks in UV-irradiated mammalian cells. Photochem Photobiol 72:477–484
Berney M, Weilenmann HU, Egli T (2007) Adaptation to UVA radiation of E. coli growing in continuous culture. J Photochem Photobiol B Biol 86:149–159
Birošová L, Mikulášová M (2009) Development of triclosan and antibiotic resistance in Salmonella enterica serovar Typhimurium. J Med Microbiol 58:436–441
Blažeka B, Šuškovič J, Matošič S (1991) Antimicrobial activity of lactobacilli and streptococci. World J Microbiol Biotechnol 7:533–536
Bradford MM (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
Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8
Chen RR (2007) Permeability issues in whole-cell bioprocess and cellular membrane engineering. Appl Microbiol Biotechnol 74:730–738
Cotter PD, Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429–453
Cronan JE Jr, Waldrop GL (2002) Multi-subunit acetyl-CoA carboxylases. Prog Lipid Res 41:407–435
Davis MS, Solbiati J, Cronan JE Jr (2000) Overproduction of acetyl-CoA carboxylase activity increases the rate of fatty acid biosynthesis in Escherichia coli. J Biol Chem 275:28593–28598
Donkor ON, Henriksson A, Vasiljevic T, Shah NP (2007) Rheological properties and sensory characteristics of set-type soy yogurt. J Agric Food Chem 55:9868–9876
Elkins CA, Mullis LB (2004) Bile-mediated aminoglycoside sensitivity in Lactobacillus species likely results from increased membrane permeability attributable to cholic acid. Appl Environ Microbiol 70:7200–7209
Ewe JA, Wan-Abdullah WN, Liong MT (2010) Viability and growth characteristics of Lactobacillus in soymilk supplemented with B-vitamins. Int J Food Sci Nutr 61:87–107
Ewe JA, Wan-Abdullah WN, Liong MT (2011) ACE inhibitory activity and bioconversion of isoflavones by Lactobacillus in soymilk supplemented with B-vitamins. Br Food J 113:1127–1146
Ewe JA, Wan-Abdullah WN, Karim AA, Liong MT (2013) Ultraviolet radiation enhanced growth of Lactobacillus and their bioconversion of isoflavones in biotin-supplemented soymilk. LWT-Food Sci Technol 50:25–31
Forestier C, De Champs C, Vatoux C, Jolie B (2000) Probiotic activities of Lactobacillus casei rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Res Microbiol 152:167–173
Gajic O, Buist G, Kojic M, Topisirovic L, Kuipers OP, Kok J (2003) Novel mechanism of bacteriocin secretion and immunity carried out by lactococcal MDR proteins. J Biol Chem 278:34291–34298
Golowczyc MA, Silva J, Teixeira P, De Antoni GL, Abraham AG (2011) Cellular injuries of spray-dried Lactobacillus spp. isolated from kefir and their impact on probiotic properties. Int J Food Microbiol 144:556–560
He YY, Klisch M, Häder DP (2002) Adaptation of cyanobacteria to UV-B stress correlated with oxidative stress and oxidative damage. Photochem Photobiol 76:188–196
Heppel LA (1969) The effect of osmotic shock on release of bacterial proteins and on active transport. J Gen Physiol 54:95–113
Herrling T, Fuchs J, Rehberg J, Groth N (2003) UV-induced free radicals in the skin detected by ESR spectroscopy and imaging using nitroxides. Free Radic Biol Med 35:59–67
Hong SI, Kim YJ, Pyun YR (1999) Acid tolerance of Lactobacillus plantarum from Kimchi. LWT-Food Sci Technol 32:142–148
Kano M, Takayanagi T, Harada K, Sawada S, Ishikawa F (2006) Bioavailability of isoflavones after ingestion of soy beverages in healthy adults. J Nutr 136:2291–2296
Kimoto H, Ohmomo S, Okamoto T (2002) Enhancement of bile tolerance in lactococci by Tween 80. J Appl Microbiol 92:41–46
Kirjavainen PV, Ouwehand AC, Isolauri E, Salminen SJ (1998) The ability of probiotic bacteria to bind to human intestinal mucus. FEMS Microbiol Lett 67:185–189
Krishnamurthy K, Tewari JC, Irudayaraj J, Demirci A (2010) Microscopic and spectroscopic evaluation of inactivation of Staphylococcus aureus by pulsed UV light and infrared heating. Food Bioprocess Technol 3:93–104
Larkin T, Price WE, Astheimer L (2008) The key importance of soy isoflavone bioavailability to understanding health benefits. Crit Rev Food Sci Nutr 48:538–552
Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ACTT 4356. Dig Dis Sci 45:1617–1622
Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47:1460–1466
Liong MT, Shah NP (2005) Production of organic acids from fermentation of mannitol, FOS and inulin by a cholesterol removing Lactobacillus acidophilus strain. J Appl Microbiol 99:783–793
Liong MT, Dunshea FR, Shah NP (2007) Effects of a synbiotic containing Lactobacillus acidophilus ATCC 4962 on plasma lipid profiles and morphology of erythrocytes in hypercholesterolaemic pigs on high- and low-fat diets. Br J Nutr 98:736–744
Liu P, Duan W, Wang Q, Li X (2010) The damage of outer membrane of Escherichia coli in the presence of TiO2 combined with UV light. Colloids Surf B: Biointerfaces 78:171–176
Mahajan PM, Desai KM, Lele SS (2012) Production of cell membrane-bound α- and β-glucosidase by Lactobacillus acidophilus. Food Bioprocess Technol 5:706–718
Matallana-Surget S, Joux F, Wattiez R, Lebaron P (2012) Proteome analysis of UVB-resistant marine bacterium Photobacterium angustum S14. PLOSone 7:e42299
Murga MLF, Bernik D, de Valdez DF, Disalvo AE (1999) Permeability and stability properties of membranes formed by lipids extracted from Lactobacillus acidophilus grown at different temperatures. Arch Biochem Biophys 364:115–121
Nagira T, Narisawa J, Teruya K, Katakura Y, Shim SY, Kusumoto K, Tokumaru S, Tokumaru S, Barnes DW, Shirahata S (2002) Suppression of UVC-induced cell damage and enhancement of DNA repair by the fermented milk, Kefir. Cytotechnology 40:125–137
Perluigi M, Di Domenico F, Blarzino C, Foppoli C, Cini C, Giorgi A, Grillo C, De Marco F, Butterfield DA, Schininà ME, Coccia R (2010) Effects of UVB-induced oxidative stress on protein expression and specific protein oxidation in normal human epithelial keratinocytes: a proteomic approach. Proteome Sci 8:1–14
Prasad J, McJarrow P, Gopal P (2003) Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69:917–925
Ren MQ, Kuhn G, Wegner J, Chen J (2001) Isoflavones, substances with multi-biological and clinical properties. Eur J Nutr 40:135–146
Schär-Zammaretti P, Ubbink J (2003) The cell wall of lactic acid bacteria: surface and macromolecular conformations. Biophys J 85:4076–4092
Schillinger U, Guigas C, Holzapfel WH (2005) In vitro adherence and other properties of lactobacilli used in probiotic yogurt-like products. Int Dairy J 15:1289–1297
Setchell KDR, Brown NM, Zimmer-Nechemias L, Brasheas WT, Wolfe BE, Krischner AS, Heubi JE (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
Shiu CT, Lee TS (2005) Ultraviolet –B-induced oxidative stress and responses of the ascorbate-glutathione cycle in a marine macroalga Ulva fasciata. J Exp Bot 56:2851–2865
Smith HL, Howland MC, Szmodis AW, Li Q, Daemon LL, Parikh AN, Majewski J (2009) Early stages of oxidative stress-induced membrane permeabilization: a neuron reflectometry study. J Am Chem Soc 131:3631–3638
Šušković J, Kos B, Beganović J, Pavunc AL, Habjanič K, Matošić S (2010) Antimicrobial activity – the most important property of probiotic and starter lactic acid bacteria. Food Technol Biotechnol 48:296–307
Teh SS, Ahmad R, Wan Abdullah WN, Liong MT (2009) Evaluation of agrowastes as immobilizers for probiotics in soymilk. J Agric Food Chem 57:10187–10198
Ukuku DO, Geveke DJ (2010) A combined treatment of UV-light and radio frequency electric field for the inactivation of Escherichia coli K-12 in apple juice. Int J Food Microbiol 138:50–55
Vaughan EE, Mollet B, Devos WM (1999) Functionality of probiotics and intestinal lactobacilli: light in the intestinal tract tunnel. Curr Opin Biotechnol 10:505–510
Wei QK, Chen TR, Chen JT (2007) Using of Lactobacillus and Bifidobacterium to product the isoflavone aglycones in fermented soymilk. Int J Food Microbiol 117:120–124
Xu GQ, Chu J, Zhuang YP, Wang YH, Zhang SL (2008) Effects of vitamins on the lactic acid biosynthesis of Lactobacillus paracasei NERCB 0401. Biochem Eng J 38:189–197
Yokota A, Veenstra M, van Kurdi P, Veen HW, Konings WN (2000) Cholate resistance in Lactococcus lactis is mediated by an ATP-dependent multispecific organic anion transporter. J Bacteriol 182:5196–5201
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The authors would like to acknowledge the financial assistance provided by Universiti Sains Malaysia via the USM RU grant (1001/PTEKIND/815056), USM IPS Research Fund grant (1002/CIPS/ATTR 3100) and the Universiti Sains Malaysia Fellowship.
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Ewe, JA., Ong, JS., Wan-Abdullah, WN. et al. Potential ramifications of the effects of sub-lethal ultraviolet B-radiation on the subsequent three subcultures of Lactobacillus fermentum BT 8219 during fermentation in biotin-supplemented soymilk and their probiotic properties. Ann Microbiol 65, 307–319 (2015). https://doi.org/10.1007/s13213-014-0863-6
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DOI: https://doi.org/10.1007/s13213-014-0863-6