Influence of pH on the Ability of Lactobacillus plantarum NB324 to Produce Conjugated Linoleic Acid
Abstract
Conjugated linoleic acid (CLA) production of lactic acid bacteria by biotransformation of linoleic acid (LA) through biohydrogenation requires the activity of linoleate isomerase (LAI). pH is known to be an important factor affecting structure and stability of this enzyme. In this research, the influence of pH on CLA production of Lactobacillus plantarum NB324 was studied, using various pH for cultivating the lactic acid bacteria. The results showed that the optimum pH for cell growth was in a range of 5.5-6.5, with a maximal cell dry weight of about 4.4 g.L-1. The highest total CLA concentration (28.2 mg.L-1) was obtained when the culture was grown at pH 5.5 The major isomer of the produced CLA was 9-CLA1, accounting for 77% of total CLA isomers. Keywords : conjugated linoleic acid, linoleic acid, Lactic acid bacteria, linoleate isomerase, Lactobacillus plantarum NB324References
AbuGhazaleh, A.A., & Jacobson, B.N. (2007). The effect of pH and polyunsaturated C18 fatty acid source on the production of vaccenic acid and conjugated linoleic acids in ruminal cultures incubated with docosahexaenoic acid. Animal Feed Science and Technology, 136, 11-22.
Belury, M.A., (2002). Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annual Review of Nutrition, 22, 505-531.
Chen, H., Yang, B., Gu, S., Zhang, B., Xu, Q., Ye, Q., Song, Y., Chen, Y.Q., Zhang, H., & Chen, W. (2012). Purification and characterization of linoleate isomerase from Lactobacillus plantarum ZS2058. African Journal of Biotechnology, 11, 4579-4587.
Choi, N.J., Imm, J.Y., Oh S., Kim, B.C., Hwang, H.J., & Kim, Y.J. (2005). Effect of pH and oxygen on conjugated linoleic acid (CLA) production by mixed rumen bacteria from cows fed high concentrate and high forage diets. Animal Feed Science and Technology, 123-124 part 2, 643-653.
Chung, S.H., Kim, I.H., Park, H.G., Kang, H.S., Yoon, C.S., Jeong, H.Y., Choi, N.J., Kwon, E.G., & Kim, Y.J. (2008). Synthesis of conjugated linoleic acid by human-derived Bifidobacterium breve LMC 017: utilization as a functional starter culture for milk fermentation. Journal of Agricultural and Food Chemistry, 56, 3311-3316.
Coakley, M., Ross, R.P., Nordgren, M., Fitzgerald, G., Devery, R., & Stanton, C. (2003). Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. Journal of Applied Microbiology, 91, 138-145.
De Man, J.C., Rogosa, M., & Sharpe, M.E. (1960.) A medium for the cultivation of lactobacilli. Journal of Bacterioogy, 23, 130.
Desbois, A.P., & Smith, V.J. (2010). Antibacterial free fatty acids: Activities, mechanisms of action and biotechnological potential. Applied Microbiology and Biotechnology, 85, 1629-1642.
Fu, W., & Mathews, A.P. (1999). Lactic acid production from lactose by Lactobacillus plantarum: kinetic model and effects of pH, substrate, and oxygen. Biochemical Engineering Journal, 3, 163–170.
Fuentes, M.C., Calsamiglia, S., Cardozo, P.W., & Vlaeminck, B. (2009). Effect of pH and level of concentrate in the diet on the production of biohydrogenation intermediates in a dual-flow continuous culture. Journal of Dairy Science, 92, 4456-4466.
Gorissen, L., Weckx, S., Vlaeminck, B., Reas, K., Vuyst, D., Smet, D., & Leroy, F. (2011). Linoleate isomerase activity occurs in lactic acid bacteria strains and is affected by pH and temperature. Journal of Applied Microbiology, 111, 593-606.
Hayek, M.G., Han, S.N., Wu, D., Watkins, B.A., Meydani, M., & Dorsey, J.L. (1999). Dietary conjugated linoleic acid influences the immune response of young and old C57BL/6NCrlBR mice. Journal of Nutrition, 129, 32-38.
Hennessy, A.A., Ross, R.P., Devery, R., & Stanton, C. (2009). Optimization of a reconstituted skim milk based medium for enhanced CLA production by bifidobacteria. Journal of Applied Microbiology, 106, 1315-1327.
Houseknecht, K.L., VandenHeuvel, J.P., Moya-Camarena, S.Y., Portocarrero, C.P., Peck, L.W., & Nickel, K.P. (1998). Dietary conjugated linoleic acid normalizes impaired glucose tolerance in the Zucker diabetic fatty fa/fa rat. Biochemical and Biophysical Research Communications, 244, 678-682.
Huang,Y.C., Luedecke, L.O., & Shultz, T.D. (1994). Effect of cheddar cheese consumption on plasma conjugated linoleic acid in men. Nutrition Research, 14, 373-386.
Hutkins, R.W., & Nannen, N.L. (1993). pH homeostasis in lactic acid bacteria. Journal of Dairy Science, 76, 2354–2365.
Ip, C., Chin, S.F., Scimeca, J.A., & Pariza, M.W. (1991). Mammary cancer prevention by conjugated dienoic derivatives of linoleic acid. Cancer Research, 51, 6118-6124.
Jenskins, J.K., & Courney, P.D. (2003). Lactobacillus growth and membrane composition in the presence of linoleic or conjugated linoleic acid. Canadian Journal of Microbiology, 49, 51-57.
Jiang, J., Bjorck, L., & Fonden, R. (1998). Production of conjugated linoleic acid by dairy starter cultures. Journal of Appllied Microbiology, 8, 95-102.
Kankaanpää, P., Yang, B. ,Kallio, H., Isolauri, E., & Salminen, S. (2004). Effect of polyunsaturated fatty acids in growth medium on lipid composition and on physicochemical surface properties of Lactobacilli. Appllied and Environmental Microbiology, 70, 129-136.
Kepler, C.R. & Tove, S.B. (1967). Biohydrogenation of unsaturated fatty acids. III. Purification and properties of a linoleate 12-cis, 11-trans-isomerase from Butyrivibrio fibrisolven. Journal of Biological Chemistry, 242(24), 5686-5692.
Kim, Y.J., Liu, R.H., Bond, D.R., & Russell, J.B. (2000). Effect of linoleic acid concentration on conjugated linoleic acid production by Butyrivibrio fibrisolvens A38. Applied and Environmental Microbiology, 66(12), 5226-5230.
Kim, Y.J., Liu, R.H., Rychlik, J.L., & Russell, J.B. (2002). The enrichment of ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10, cis-12 isomer of conjugated linoleic acid. Journal of Applied Microbiology, 92, 976-982.
Kim, Y.J. & Liu, R.H. (2002). Increase of conjugated linoleic acid content in milk by fermentation with lactic acid bacteria. Journal of Food Science, 67(5), 1731-1737.
Kishino, S., Ogawa, J., Ando, A., Omura, Y., & Shimizu, S. (2002). Ricinoleic acid and castor oil as substrates for conjugated linoleic acid production by washed cells of Lactobacillus plantarum. Bioscience, Biotechnology and Biochemistry, 66, 2283-2286.
Kritchevsky, D., Tepper, S.A., Wright, S., & Czarnecki, S.K. (2002). Influence of graded levels of conjugated linoleic acid (CLA) on experimental atherosclerosis in rabbits. Nutrition Research, 22, 1275-1279.
LeBlanc, J.G., Garro, M.S., & Savoy, de Giori G., (2004). Effect of pH on Lactobacillus fermentum growth, raffinose removal, -galactosidase activity and fermentation product. Applied Microbiology and Biotechnology, 65, 265-271.
Li, J., Zhang, L., Han, X., Yi, H., Guo, C., Zhang, Y., Du, M., Luo, X., Zhang, Y., & Shan, Y. (2013). Effect of incubation conditions and possible intestinal nutrients on cis-9, trans-11 conjugated linoleic acid production by Lactobacillus acidophilus F0221. International Dairy Journal, 29, 93-98.
Lin, T.Y., Lin, C.W., & Wang, Y.J. (2002). Linoleic acid isomerase activity in enzyme extracts from Lactobacillus acidophilus and Propionibacterium freudenreichii ssp. shermanii. Journal of Food Science, 67, 1502-1505.
Liu, P., Shen, S.R., Ruan, H., Zhou, Q., Ma, L.L., & He, G. Q. (2011). Production of conjugated linoleic acids by Lactobacillus plantarum strains isolated from naturally fermented Chinese pickles. Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology), 12(11), 923- 930.
Matagaras, M., Metaxopoulos, J., Galiotou, M., & Drosinos, EH. (2003). Influence of pH and temperature on growth and bacteriocin production by Leuconostoc mesenteroides L124 and Lactobacillus curvatus L442. Meat Science, 64, 265-271.
Mulvihill, B. (2001). Ruminant meat as a source of conjugated linoleic acid (CLA). Nutrition Bulletin, 26, 295-299.
Ogawa, J., Kishino, S., Ando, A., Sugimoto, S., Mihara, K., & Shimizu, S. (2005). Production of conjugated fatty acids by lactic acid bacteria. Journal of Bioscience and Bioengineering, 100, 355-364.
Oh, D.K., Hong, G.H., Lee, Y., Min, S.G., Sin, H.S., & Cho, S.K. (2003). Production of conjugated linoleic acid by isolated Bifidobacterium strains. World Journal of Microbiology and Biotechnology, 19, 907-912.
Partanen, L., Marttinen, N., & Alatossava, T. (2001). Fats and fatty acids as growth factors for Lactobacillus delbrueckii. Syst. Appliled Microbiology, 24, 500-506.
Rainio, A., Vahvaselkä, M.,Suomalainen, T., & Laakso, S. (2001). Reduction of linoleic acid inhibition inproduction of conjugated linoleic acid by Propionibacterium freudenreichii ssp. shermanii. Canadian Journal of Microbiology, 47, 735-740.
Rodríguez-Alcalá, L.M., Braga, T., Xavier Malcata, F., Gomes, A., & Fontecha, J. (2011). Quantitative and qualitative determination of CLA produced by Bifidobacterium and lactic acid bacteria by combining spectrophotometric and Ag +-HPLC techniques. Food Chemistry, 125(4), 1373-1378.
Schmid, A., Collomb, M., Sieber, R., & Bee, G. (2006). Conjugated linoleic acid in meat and meat products: a review. Meat Science, 73, 29-41.
Sieber, R., Collomb, M., Aeschlimann, A., Jelen, P., & Eyer, H. (2004). Impact of microbial cultures on conjugated linoleic acid in dairy products- a review. International Dairy Journal, 14, 1-15.
Soto, C. (2013). Lactobacillus plantarum as source of conjugated linoleic acid: Effect of pH, incubation temperature and inulin incorporation. Journal of Biochemical Technology, 5, 649-653.
Troegeler-Meynadier, A., Nicot, M.C., Bayourthe, C., Moncoulon, R., & Enjalbert, F. (2003). Effect of pH and concentrations of linoleic and linolenic acids on extent and intermediated of ruminal biohydrogenation in vitro. Journal of Dairy Science, 86, 4054-4063.
Van Nieuwenhove, C.P., Oliszewski, R., Gonzalez, S.N., & Perez Chaia, A.B., (2007). Conjugated linoleic acid conversion by dairy bacteria cultured in MRS broth and buffalo milk. Letters in Applied Microbiology, 44(5), 467-474.
Xu, S., Boylston, T., & Glatz, B. (2004). Effect of lipid source on probiotic bacteria and conjugated linoleic acid formation in milk model systems. Journal of the American Oil Chemists’ Society, 81, 589-595.
Yurawecz, M., Mossoba, M., Kramer, J., Pariza, M., & Nelson, G. (1999). Advances in conjugated linoleic acid research. AOCS Press, Champaign, Illinois, USA.
Belury, M.A., (2002). Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annual Review of Nutrition, 22, 505-531.
Chen, H., Yang, B., Gu, S., Zhang, B., Xu, Q., Ye, Q., Song, Y., Chen, Y.Q., Zhang, H., & Chen, W. (2012). Purification and characterization of linoleate isomerase from Lactobacillus plantarum ZS2058. African Journal of Biotechnology, 11, 4579-4587.
Choi, N.J., Imm, J.Y., Oh S., Kim, B.C., Hwang, H.J., & Kim, Y.J. (2005). Effect of pH and oxygen on conjugated linoleic acid (CLA) production by mixed rumen bacteria from cows fed high concentrate and high forage diets. Animal Feed Science and Technology, 123-124 part 2, 643-653.
Chung, S.H., Kim, I.H., Park, H.G., Kang, H.S., Yoon, C.S., Jeong, H.Y., Choi, N.J., Kwon, E.G., & Kim, Y.J. (2008). Synthesis of conjugated linoleic acid by human-derived Bifidobacterium breve LMC 017: utilization as a functional starter culture for milk fermentation. Journal of Agricultural and Food Chemistry, 56, 3311-3316.
Coakley, M., Ross, R.P., Nordgren, M., Fitzgerald, G., Devery, R., & Stanton, C. (2003). Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. Journal of Applied Microbiology, 91, 138-145.
De Man, J.C., Rogosa, M., & Sharpe, M.E. (1960.) A medium for the cultivation of lactobacilli. Journal of Bacterioogy, 23, 130.
Desbois, A.P., & Smith, V.J. (2010). Antibacterial free fatty acids: Activities, mechanisms of action and biotechnological potential. Applied Microbiology and Biotechnology, 85, 1629-1642.
Fu, W., & Mathews, A.P. (1999). Lactic acid production from lactose by Lactobacillus plantarum: kinetic model and effects of pH, substrate, and oxygen. Biochemical Engineering Journal, 3, 163–170.
Fuentes, M.C., Calsamiglia, S., Cardozo, P.W., & Vlaeminck, B. (2009). Effect of pH and level of concentrate in the diet on the production of biohydrogenation intermediates in a dual-flow continuous culture. Journal of Dairy Science, 92, 4456-4466.
Gorissen, L., Weckx, S., Vlaeminck, B., Reas, K., Vuyst, D., Smet, D., & Leroy, F. (2011). Linoleate isomerase activity occurs in lactic acid bacteria strains and is affected by pH and temperature. Journal of Applied Microbiology, 111, 593-606.
Hayek, M.G., Han, S.N., Wu, D., Watkins, B.A., Meydani, M., & Dorsey, J.L. (1999). Dietary conjugated linoleic acid influences the immune response of young and old C57BL/6NCrlBR mice. Journal of Nutrition, 129, 32-38.
Hennessy, A.A., Ross, R.P., Devery, R., & Stanton, C. (2009). Optimization of a reconstituted skim milk based medium for enhanced CLA production by bifidobacteria. Journal of Applied Microbiology, 106, 1315-1327.
Houseknecht, K.L., VandenHeuvel, J.P., Moya-Camarena, S.Y., Portocarrero, C.P., Peck, L.W., & Nickel, K.P. (1998). Dietary conjugated linoleic acid normalizes impaired glucose tolerance in the Zucker diabetic fatty fa/fa rat. Biochemical and Biophysical Research Communications, 244, 678-682.
Huang,Y.C., Luedecke, L.O., & Shultz, T.D. (1994). Effect of cheddar cheese consumption on plasma conjugated linoleic acid in men. Nutrition Research, 14, 373-386.
Hutkins, R.W., & Nannen, N.L. (1993). pH homeostasis in lactic acid bacteria. Journal of Dairy Science, 76, 2354–2365.
Ip, C., Chin, S.F., Scimeca, J.A., & Pariza, M.W. (1991). Mammary cancer prevention by conjugated dienoic derivatives of linoleic acid. Cancer Research, 51, 6118-6124.
Jenskins, J.K., & Courney, P.D. (2003). Lactobacillus growth and membrane composition in the presence of linoleic or conjugated linoleic acid. Canadian Journal of Microbiology, 49, 51-57.
Jiang, J., Bjorck, L., & Fonden, R. (1998). Production of conjugated linoleic acid by dairy starter cultures. Journal of Appllied Microbiology, 8, 95-102.
Kankaanpää, P., Yang, B. ,Kallio, H., Isolauri, E., & Salminen, S. (2004). Effect of polyunsaturated fatty acids in growth medium on lipid composition and on physicochemical surface properties of Lactobacilli. Appllied and Environmental Microbiology, 70, 129-136.
Kepler, C.R. & Tove, S.B. (1967). Biohydrogenation of unsaturated fatty acids. III. Purification and properties of a linoleate 12-cis, 11-trans-isomerase from Butyrivibrio fibrisolven. Journal of Biological Chemistry, 242(24), 5686-5692.
Kim, Y.J., Liu, R.H., Bond, D.R., & Russell, J.B. (2000). Effect of linoleic acid concentration on conjugated linoleic acid production by Butyrivibrio fibrisolvens A38. Applied and Environmental Microbiology, 66(12), 5226-5230.
Kim, Y.J., Liu, R.H., Rychlik, J.L., & Russell, J.B. (2002). The enrichment of ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10, cis-12 isomer of conjugated linoleic acid. Journal of Applied Microbiology, 92, 976-982.
Kim, Y.J. & Liu, R.H. (2002). Increase of conjugated linoleic acid content in milk by fermentation with lactic acid bacteria. Journal of Food Science, 67(5), 1731-1737.
Kishino, S., Ogawa, J., Ando, A., Omura, Y., & Shimizu, S. (2002). Ricinoleic acid and castor oil as substrates for conjugated linoleic acid production by washed cells of Lactobacillus plantarum. Bioscience, Biotechnology and Biochemistry, 66, 2283-2286.
Kritchevsky, D., Tepper, S.A., Wright, S., & Czarnecki, S.K. (2002). Influence of graded levels of conjugated linoleic acid (CLA) on experimental atherosclerosis in rabbits. Nutrition Research, 22, 1275-1279.
LeBlanc, J.G., Garro, M.S., & Savoy, de Giori G., (2004). Effect of pH on Lactobacillus fermentum growth, raffinose removal, -galactosidase activity and fermentation product. Applied Microbiology and Biotechnology, 65, 265-271.
Li, J., Zhang, L., Han, X., Yi, H., Guo, C., Zhang, Y., Du, M., Luo, X., Zhang, Y., & Shan, Y. (2013). Effect of incubation conditions and possible intestinal nutrients on cis-9, trans-11 conjugated linoleic acid production by Lactobacillus acidophilus F0221. International Dairy Journal, 29, 93-98.
Lin, T.Y., Lin, C.W., & Wang, Y.J. (2002). Linoleic acid isomerase activity in enzyme extracts from Lactobacillus acidophilus and Propionibacterium freudenreichii ssp. shermanii. Journal of Food Science, 67, 1502-1505.
Liu, P., Shen, S.R., Ruan, H., Zhou, Q., Ma, L.L., & He, G. Q. (2011). Production of conjugated linoleic acids by Lactobacillus plantarum strains isolated from naturally fermented Chinese pickles. Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology), 12(11), 923- 930.
Matagaras, M., Metaxopoulos, J., Galiotou, M., & Drosinos, EH. (2003). Influence of pH and temperature on growth and bacteriocin production by Leuconostoc mesenteroides L124 and Lactobacillus curvatus L442. Meat Science, 64, 265-271.
Mulvihill, B. (2001). Ruminant meat as a source of conjugated linoleic acid (CLA). Nutrition Bulletin, 26, 295-299.
Ogawa, J., Kishino, S., Ando, A., Sugimoto, S., Mihara, K., & Shimizu, S. (2005). Production of conjugated fatty acids by lactic acid bacteria. Journal of Bioscience and Bioengineering, 100, 355-364.
Oh, D.K., Hong, G.H., Lee, Y., Min, S.G., Sin, H.S., & Cho, S.K. (2003). Production of conjugated linoleic acid by isolated Bifidobacterium strains. World Journal of Microbiology and Biotechnology, 19, 907-912.
Partanen, L., Marttinen, N., & Alatossava, T. (2001). Fats and fatty acids as growth factors for Lactobacillus delbrueckii. Syst. Appliled Microbiology, 24, 500-506.
Rainio, A., Vahvaselkä, M.,Suomalainen, T., & Laakso, S. (2001). Reduction of linoleic acid inhibition inproduction of conjugated linoleic acid by Propionibacterium freudenreichii ssp. shermanii. Canadian Journal of Microbiology, 47, 735-740.
Rodríguez-Alcalá, L.M., Braga, T., Xavier Malcata, F., Gomes, A., & Fontecha, J. (2011). Quantitative and qualitative determination of CLA produced by Bifidobacterium and lactic acid bacteria by combining spectrophotometric and Ag +-HPLC techniques. Food Chemistry, 125(4), 1373-1378.
Schmid, A., Collomb, M., Sieber, R., & Bee, G. (2006). Conjugated linoleic acid in meat and meat products: a review. Meat Science, 73, 29-41.
Sieber, R., Collomb, M., Aeschlimann, A., Jelen, P., & Eyer, H. (2004). Impact of microbial cultures on conjugated linoleic acid in dairy products- a review. International Dairy Journal, 14, 1-15.
Soto, C. (2013). Lactobacillus plantarum as source of conjugated linoleic acid: Effect of pH, incubation temperature and inulin incorporation. Journal of Biochemical Technology, 5, 649-653.
Troegeler-Meynadier, A., Nicot, M.C., Bayourthe, C., Moncoulon, R., & Enjalbert, F. (2003). Effect of pH and concentrations of linoleic and linolenic acids on extent and intermediated of ruminal biohydrogenation in vitro. Journal of Dairy Science, 86, 4054-4063.
Van Nieuwenhove, C.P., Oliszewski, R., Gonzalez, S.N., & Perez Chaia, A.B., (2007). Conjugated linoleic acid conversion by dairy bacteria cultured in MRS broth and buffalo milk. Letters in Applied Microbiology, 44(5), 467-474.
Xu, S., Boylston, T., & Glatz, B. (2004). Effect of lipid source on probiotic bacteria and conjugated linoleic acid formation in milk model systems. Journal of the American Oil Chemists’ Society, 81, 589-595.
Yurawecz, M., Mossoba, M., Kramer, J., Pariza, M., & Nelson, G. (1999). Advances in conjugated linoleic acid research. AOCS Press, Champaign, Illinois, USA.
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2016-02-02
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