Effects of pH, temperature and salt on antagonistic activity of barley sourdough lactic acid bacteria on Bacillus subtilis and evaluation of serum parameters and liver enzymes in mice fed with LAB isolates
Subject Areas :
Food Science and Technology
M. Ebrahimi
1
,
Maryam Khashaie
2
,
Farzaneh KiaDaliri
3
,
Alireza Sadeghi
4
1 - Assistant Professor, Cereal Health Research Centre, Golestan University of Medical Science, Gorgan, Iran
2 - Former MSc student of Food Biotechnology, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources
3 - Former MSc student of Food Biotechnology, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources
4 - Assistant Professor, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources
Received: 2017-03-04
Accepted : 2019-07-10
Published : 2019-06-22
Keywords:
sourdough,
biopreservative,
LAB isolates,
Abstract :
In this experimental study, the effect of pH (2, 4, 11), temperature (4, 85, 121 oC) and bile salt (0.3, 0.6, 1%) treatments on inhibitory potential of cell-free supernatant (CFS) obtained from barley sourdough dominant LAB (Pediococcus stilesii, Weissella cibaria, Lactobacillus brevis and Lactobacillus curieae) isolates, against B. subtilis were investigated based on microdilution method in comparison to untreated CFS. The safety of LAB isolates was also assessed by control of changes in serum parameters and liver enzymes in mice fed with them. Results were analyzed by one-way analysis of variance. Based on results, LAB CFS had antagonistic activity against B. subtilis. Inhibitory effects of the CFS under pH and temperature treatments were decreased, but under bile salt treatment was increased. Changes in serum parameters and liver enzymes in mice fed with LAB isolates were also in normal ranges and so on, safety of the LAB isolates was approved. By considering the antagonistic activity of LAB CFS under pH, temperature and salt treatments, against B. subtilis it is possible to use from the CFS as a biopreservative in food processing chain.
References:
· sefa, E., Beyene, F., Santhanam, A. (2008). Effect of temperature and pH on the antimicrobial activity of inhibitory substances produced by lactic acid bacteria isolated from Ergo, an Ethiopian traditional fermented milk. African Journal of Microbiology Research, 2(9): 229-234.
· Cizeikiene, D., Juodeikiene, G., Paskericius, A., Bartkiene, E. (2013). Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control, 31(2): 539-545.
· Corsetti, A., Gobbetti, M., Smacchi, E. (1996). Antibacterial activity of sourdough lactic acid bacteria: isolation of a bacteriocin like inhibitory substance from Lactobacillus sanfrancisco C57. Food Microbiology, 13(6): 447-456.
· Corsetti, A., Settanni, L., Van Sinderen, D. (2004). Characterization of bacteriocin-like inhibitory substances (BLIS) from sourdough lactic acid bacteria and evaluation of their in vitro and in situ activity. Journal of Applied Microbiology, 96(3): 521-534.
· Digaitiene, A., Hansen, A.S., Juodeikiene, G., Eidukonyte, D., Josephsen, J. (2012). Lactic acid bacteria isolated from rye sourdoughs produce bacteriocin-like inhibitory substances active against Bacillus subtilis and fungi. Journal of Applied Microbiology, 112(4): 732-742.
· Havelaar, A.H., Brul, S., Jong, A.D., Jonge, R.D., Zwietering, M.H., ter Kuile, B.H. (2010). Future challenges to microbial food safety. International Journal of Food Microbiology, 139: S79-S94.
· Juarez Tomas, M.S., Bru, E., Wiese, B., de Ruiz Holgado, A.A.P, Nader-Macıas, M.E. (2002). Influence of pH, temperature and culture media on the growth and bacteriocin production by vaginal Lactobacillus salivarius CRL 1328. Journal of Applied Microbiology, 93(4): 714-724.
· Katina, K., Sauri, M., Alakomi, H.L., Sandholm, T.M. (2002). Potential of lactic acid bacteria to inhibit rope spoilage in wheat sourdough bread. LWT-Food Science and Technology, 35(1): 38-45.
· Katina, K. (2005). Sourdough a tool for the improved flavour, texture and shelf-life of wheat bread.VTT Technology Research Center of Finland. 569: 13-41.
· Lavermicocca, P., Valerio, F., Visconti, A. (2003). Antifungal activity of phenyl lactic acid against molds isolated from bakery products. Applied and Environmental Microbiology, 69(1): 634-640.
· Leroy, F., De Vuyst, L. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends in Food Science & Technology, 15(2): 67-78.
· Leroy, F., De Vuyst, L. (1999). The presence of salt and a curing agent reduces bacteriocin production by Lactobacillus sakei CTC494, a potential starter culture for sausage fermentation. Applied and Environmental Microbiology, 65(12): 5350-5356.
· Li, D., Ni, K., Pang, H., Wang, Y., Cai, Y., Jin, Q. (2015). Identification and antimicrobial activity detection of lactic acid bacteria isolated from corn stover silage. Asian Australians Journal of Animal Science, 28(5): 620-631.
· Mentes, O., Ercan, R., Akcelik, M. (2007). Inhibitor activities of two lactobacillus strains, isolated from sourdough, against rope forming bacillus strains. Food Control, 18(4): 359-363.
· Messens, W., De Vuyest, L. (2002). Inhibitory substances produced by Lactobacilli isolated from sourdough- a review. International Journal of Food Microbiology, 72(1-2): 31-43.
· Millette, M., Dupon, C., Archambault, D., Lacroix, M. (2007). Partial characterization of bacteriocins produced by human Lactococcus lactis and Pediococcus acidilactici isolates. Journal of Applied Microbiology, 102(1): 274-282.
· Mohsen, S.M., Aly, M.H., Attia, A.A., Osman, D.B. (2016). Effect of sourdough on shelf life, freshness and sensory characteristics of Egyptian balady bread.Journal of Applied and Environmental Microbiology, 4(2): 39-45.
· Neysens, P., Messens, W., De Vuyst, L. (2003). Effect of sodium chloride on growth and bacteriocin production by Lactobacillus amylovorus DCE 471. International Journal of Food Microbiology, 88(1): 29-39.
· Noordiana, N., Fatimah, A.B., Mun, A.S. (2013). Antibacterial agents produced by lactic acid bacteria isolated from threadfin salmon and grass shrimp. International Food Research Journal, 20(1): 117-124.
· Pepe, O., Blaiotta, G., Moschetti, G., Greco, T., Villani, F. (2003). Rope producing strains of Bacillus spp. from wheat bread and strategy for their control by lactic acid bacteria.Applied and Environmental Microbiology, 69(4): 2321-2329.
· Rozes, N., Peres, C. (1996). Effect of oleuropein and sodium chloride on viability and metabolism of Lactobacillus plantarum. Applied Microbiology and Biotechnology, 45(6): 839-843.
· Sadeghi, A., Raeisi, M., Ebrahimi, M. (2017). Sourdough: functional feathers and healthy benefits. Golestan University of Medical Sciences Press, 35-57, ISSN 97860095473-33 [In Persian].
· Settanni, L., Valmorri, S., Suzzi, G., Corsetti, A. (2008). The role of environmental factors and medium composition on bacteriocin-like inhibitory substances (BLIS) production by Enterococcus mundtii strains. Food Microbiology, 25(5): 722-728.
· Simsek, O., Hilmi Con, A., Tumuloglu, S. (2006). Isolating lactic starter cultures with antimicrobial activity for sourdough process. Food Control, 17(4): 263-270.
· Suskovic, J., Kos, B., Beganovic, J., Pavunc, A.L., Habjanic, K., Matosic, S. (2010). Antimicrobial activity, the most important property of probiotic and starter lactic acid bacteria. Food Technology and Biotechnology, 48(3): 296-307.
· Szabo, N.J., Dolan, L.C., Burdock, G.A., Shibano, T., Sato, S., Suzuki, H., et al. (2011). Safety evaluation of Lactobacillus pentosus strain b240. Food Chemistry and Toxicology, 49(1): 251-258.
· Todorov, S.D., Dicks, L.M.T. (2005). Pediocin ST18, an anti Listerial bacteriocin produced by Pediococcus pentosaceus ST18 isolated from boza, a traditional cereal beverage from Bulgaria. Process Biochemistry, 40(1): 365-370.
· Tsai, C.C., Leu, S.F., Huang, Q.R., Chou, L.C., Huang, C.C. (2014). Safety evaluation of multiple strains of Lactobacillus plantarum and Pediococcus pentosaceus in wistar rats based on the Ames test and a 28-day feeding study. Science World Journal, 2014: 1-9.
· Valerio, F., De Bellis, P., Lonigro, S.L., Visconti, A., Lavermicocca, P. (2008). Use of Lactobacillus plantarum fermentation products in bread-making to prevent Bacillus subtilis ropy spoilage. International Journal of Food Microbiology, 122(3): 328-332.
· Vanderbergh, P.A. (1993). Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiology Review, 12(1-3): 221-237.
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· sefa, E., Beyene, F., Santhanam, A. (2008). Effect of temperature and pH on the antimicrobial activity of inhibitory substances produced by lactic acid bacteria isolated from Ergo, an Ethiopian traditional fermented milk. African Journal of Microbiology Research, 2(9): 229-234.
· Cizeikiene, D., Juodeikiene, G., Paskericius, A., Bartkiene, E. (2013). Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control, 31(2): 539-545.
· Corsetti, A., Gobbetti, M., Smacchi, E. (1996). Antibacterial activity of sourdough lactic acid bacteria: isolation of a bacteriocin like inhibitory substance from Lactobacillus sanfrancisco C57. Food Microbiology, 13(6): 447-456.
· Corsetti, A., Settanni, L., Van Sinderen, D. (2004). Characterization of bacteriocin-like inhibitory substances (BLIS) from sourdough lactic acid bacteria and evaluation of their in vitro and in situ activity. Journal of Applied Microbiology, 96(3): 521-534.
· Digaitiene, A., Hansen, A.S., Juodeikiene, G., Eidukonyte, D., Josephsen, J. (2012). Lactic acid bacteria isolated from rye sourdoughs produce bacteriocin-like inhibitory substances active against Bacillus subtilis and fungi. Journal of Applied Microbiology, 112(4): 732-742.
· Havelaar, A.H., Brul, S., Jong, A.D., Jonge, R.D., Zwietering, M.H., ter Kuile, B.H. (2010). Future challenges to microbial food safety. International Journal of Food Microbiology, 139: S79-S94.
· Juarez Tomas, M.S., Bru, E., Wiese, B., de Ruiz Holgado, A.A.P, Nader-Macıas, M.E. (2002). Influence of pH, temperature and culture media on the growth and bacteriocin production by vaginal Lactobacillus salivarius CRL 1328. Journal of Applied Microbiology, 93(4): 714-724.
· Katina, K., Sauri, M., Alakomi, H.L., Sandholm, T.M. (2002). Potential of lactic acid bacteria to inhibit rope spoilage in wheat sourdough bread. LWT-Food Science and Technology, 35(1): 38-45.
· Katina, K. (2005). Sourdough a tool for the improved flavour, texture and shelf-life of wheat bread.VTT Technology Research Center of Finland. 569: 13-41.
· Lavermicocca, P., Valerio, F., Visconti, A. (2003). Antifungal activity of phenyl lactic acid against molds isolated from bakery products. Applied and Environmental Microbiology, 69(1): 634-640.
· Leroy, F., De Vuyst, L. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends in Food Science & Technology, 15(2): 67-78.
· Leroy, F., De Vuyst, L. (1999). The presence of salt and a curing agent reduces bacteriocin production by Lactobacillus sakei CTC494, a potential starter culture for sausage fermentation. Applied and Environmental Microbiology, 65(12): 5350-5356.
· Li, D., Ni, K., Pang, H., Wang, Y., Cai, Y., Jin, Q. (2015). Identification and antimicrobial activity detection of lactic acid bacteria isolated from corn stover silage. Asian Australians Journal of Animal Science, 28(5): 620-631.
· Mentes, O., Ercan, R., Akcelik, M. (2007). Inhibitor activities of two lactobacillus strains, isolated from sourdough, against rope forming bacillus strains. Food Control, 18(4): 359-363.
· Messens, W., De Vuyest, L. (2002). Inhibitory substances produced by Lactobacilli isolated from sourdough- a review. International Journal of Food Microbiology, 72(1-2): 31-43.
· Millette, M., Dupon, C., Archambault, D., Lacroix, M. (2007). Partial characterization of bacteriocins produced by human Lactococcus lactis and Pediococcus acidilactici isolates. Journal of Applied Microbiology, 102(1): 274-282.
· Mohsen, S.M., Aly, M.H., Attia, A.A., Osman, D.B. (2016). Effect of sourdough on shelf life, freshness and sensory characteristics of Egyptian balady bread.Journal of Applied and Environmental Microbiology, 4(2): 39-45.
· Neysens, P., Messens, W., De Vuyst, L. (2003). Effect of sodium chloride on growth and bacteriocin production by Lactobacillus amylovorus DCE 471. International Journal of Food Microbiology, 88(1): 29-39.
· Noordiana, N., Fatimah, A.B., Mun, A.S. (2013). Antibacterial agents produced by lactic acid bacteria isolated from threadfin salmon and grass shrimp. International Food Research Journal, 20(1): 117-124.
· Pepe, O., Blaiotta, G., Moschetti, G., Greco, T., Villani, F. (2003). Rope producing strains of Bacillus spp. from wheat bread and strategy for their control by lactic acid bacteria.Applied and Environmental Microbiology, 69(4): 2321-2329.
· Rozes, N., Peres, C. (1996). Effect of oleuropein and sodium chloride on viability and metabolism of Lactobacillus plantarum. Applied Microbiology and Biotechnology, 45(6): 839-843.
· Sadeghi, A., Raeisi, M., Ebrahimi, M. (2017). Sourdough: functional feathers and healthy benefits. Golestan University of Medical Sciences Press, 35-57, ISSN 97860095473-33 [In Persian].
· Settanni, L., Valmorri, S., Suzzi, G., Corsetti, A. (2008). The role of environmental factors and medium composition on bacteriocin-like inhibitory substances (BLIS) production by Enterococcus mundtii strains. Food Microbiology, 25(5): 722-728.
· Simsek, O., Hilmi Con, A., Tumuloglu, S. (2006). Isolating lactic starter cultures with antimicrobial activity for sourdough process. Food Control, 17(4): 263-270.
· Suskovic, J., Kos, B., Beganovic, J., Pavunc, A.L., Habjanic, K., Matosic, S. (2010). Antimicrobial activity, the most important property of probiotic and starter lactic acid bacteria. Food Technology and Biotechnology, 48(3): 296-307.
· Szabo, N.J., Dolan, L.C., Burdock, G.A., Shibano, T., Sato, S., Suzuki, H., et al. (2011). Safety evaluation of Lactobacillus pentosus strain b240. Food Chemistry and Toxicology, 49(1): 251-258.
· Todorov, S.D., Dicks, L.M.T. (2005). Pediocin ST18, an anti Listerial bacteriocin produced by Pediococcus pentosaceus ST18 isolated from boza, a traditional cereal beverage from Bulgaria. Process Biochemistry, 40(1): 365-370.
· Tsai, C.C., Leu, S.F., Huang, Q.R., Chou, L.C., Huang, C.C. (2014). Safety evaluation of multiple strains of Lactobacillus plantarum and Pediococcus pentosaceus in wistar rats based on the Ames test and a 28-day feeding study. Science World Journal, 2014: 1-9.
· Valerio, F., De Bellis, P., Lonigro, S.L., Visconti, A., Lavermicocca, P. (2008). Use of Lactobacillus plantarum fermentation products in bread-making to prevent Bacillus subtilis ropy spoilage. International Journal of Food Microbiology, 122(3): 328-332.
· Vanderbergh, P.A. (1993). Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiology Review, 12(1-3): 221-237.