GROWTH ABILITY OF BACTERIOCINOGENIC STRAINS IN MILK AND THEIR BACTERIOCIN ACTIVITY AGAINST CHEESE STARTER CULTURES
Year 2020,
Volume: 45 Issue: 6, 1175 - 1187, 12.10.2020
Nilgün Öncül
,
Zeliha Yıldırım
Abstract
In this study, the growing ability of Lactococcus lactis ssp. lactis BZ and Enterococcus faecalis KP in different fat content milk at 30°C for 48 hours and the efficiency of their bacteriocins, lactococcin BZ and enterocin KP, against three types of cheese starter (Choozit MA 11LYO 50, Choozit MA 19LYO 50 and DI-Prox M265) in full fat milk were determined. The growth and bacteriocin production abilities of L. lactis ssp. lactis BZ and E. faecalis KP in milk were examined for 48 hours at 30°C. As a result of the study, it was determined that both bacteria grew better in milk with low fat content and produced more bacteriocin. It was found that lactococcin BZ (1600 AU/mL) and enterocin KP (1600 AU/mL) had an inhibitory effect against three different cheese starter cultures analyzed when used separately or in combination.
Supporting Institution
Gaziosmanpaşa Üniversitesi
Thanks
This work was supported by the Gaziosmanpasa University, Turkey [grant number 2008-50].
References
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- AOAC (1995). Official methods of analysis of AOAC INTERNATIONAL, 16th Edition, Washington, D.C., the USA.
- Ávila, M., Gómez‐Torres, N., Gaya, P., Garde, S. (2020). Effect of a nisin‐producing lactococcal starter on the late blowing defect of cheese caused by Clostridium tyrobutyricum. Int J Food Scı Tech 1-7, doi.org/10.1111/ijfs.14598.
- Beasley, S. (2004). Isolation, identification and exploitation lactic acid bacteria from human and animal microbiota. University of Helsinki, Faculty of Agriculture and Forestry and Viikki Graduate School in Biosciences, Department of Applied Chemistry and Microbiology Division of Microbiology, Academic Dissertation, Helsinki, Finland, 57 pages.
- Benmouna1, Z., Dalache, F., Karam, N., Zadi-Karam, H. (2018). Optimization and some characteristics of bacteriocin produced by Enterococcus sp. CM9 collected from Mauritanian Camel milk. Emir J Food Agr 30(4): 275-282, DOI https://doi.org/10.9755/ejfa.2018.v30.i4.1662.
- Bizani, D., Morrissy, J.A.C., Dominguez, A.P.M., Brandelli, A. (2008). Inhibition of Listeria monocytogenes in dairy products using the bacteriocin-like peptide cerein 8A. Int. J. Food Microbiol., 121 (2): 229–233, doi.org/10.1016/j.ijfoodmicro.2007.11.016.
- Chen, H., Hoover, D.G. (2003). Bacteriocins and their food applications. Compr. Rev. Food Sci. Food Saf. 2: 82-100, doi.org/10.1111/j.1541-4337.2003.tb00016.x.
- Cintas, L.M., Casaus, M.P., Herranz, C., Nes, I.F., Hernández, P.E. (2001). Review: bacteriocins of lactic acid bacteria. Food Sci Technol Int, 7 (4): 281-305, doi.org/10.1106/R8DE-P6HU-CLXP-5RYT.
- Cleveland, J., Montville, T.J., Nes, I.F., Chikindas, M.L. (2001). Bacteriocins: safe, natural antimicrobials for food preservation. Int. J. Food Microbiol., 71, 1-20, doi.org/10.1016/S0168-1605(01)00560-8.
- De Vuyst, L., Leroy, F. (2007). Bacteriocins from lactic acid bacteria: production, purification, and food application. J Mol Microbiol Biotechnol, 13: 194-199, doi.org/10.1159/000104752.
- Deegan, L.H., Cotter, P.D., Hill, C., Ross, P. (2006). Bacteriocins: biological tools for biopreservation and shelf-life extension. Int. Dairy J. 16: 1058–1071, doi.org/10.1016/j.idairyj.2005.10.026.
- Eissa, S. A., Elbarbary, H. A., Ibrahim, E., & Mohammed, H. A. (2018). Growth pattern of starter cultures and antifungal activity of some bacteriocins and ınulin in skim milk yoghurt. Alex. J. Vet. Sci., 59 (2): 17-25, DOI: 10.5455/ajvs.12522
- Foulquie Moreno, M.R., Callewaert, R., Devreese, B., Beeumen, J.V., De Vuyst, L. (2003). Isolation and biochemical characterisation of enterocins produced by enterococci from different sources. J. Appl. Microbiol, 94: 214-229.
- Galvez, A., Abriouel, H., Lopez, R.L., Omar, N.B. (2007). Bacteriocin-based strategies for food biopreservation. Int. J. Food Microbiol., 120: 51-70.
- Garde, S., Ávila, M., Arias, R., Gaya, P., Nuñez, M. (2011). Outgrowth inhibition of Clostridium beijerinckii spores by a bacteriocin-producing lactic culture in ovine milk cheese. Int. J. Food Microbiol., 150: 59–65.
- Isleroglu, H., Yildirim, Z., Tokatli, M., Oncul, N., Yildirim, M. (2012). Partial characterisation of enterocin KP produced by Enterococcus faecalis KP, a cheese isolate. Int. J. Dairy Technol., 65: 90-97.
- Khalid, F., Siddiqi, R., Mojgani, N. (1999). Detection and characterization of a heat stable bacteriocin (lactocin Lc-09) produced by a clinical isolate of lactobacilli. Med. J. İslamic World Acad. Sci. 12 (3): 67-71.
- Klaenhammer, T.R. (1993). Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Lett., 12: 39-86, doi.org/10.1111/j.1574-6976.1993.tb00012.x
- Kuipers, O.P.P., Ruyter, G.G., Kleerebezem, A.M., Vos, W.M. (1997). Controlled overproduction of proteins by lactic acid bacteria. Trends Biotechnol., 15: 135-140, doi.org/10.1016/S0167-7799(97)01029-9.
- Lacrois, I.C. (2008). Cheese cultures: From just acidification to complex functionalities. 5th DF Symposium on Cheese Ripening, 9-13 March, 2008, Bern, Switzeland.
- Lauková, A., Czikková, S. (2001). Antagonistic effect of enterocin CCM 4231 from Enterococcus faecium on “bryndza”, a traditional Slovak dairy product from sheep milk. Microbiol. Res, 156: 31- 34, doi.org/10.1078/0944-5013-00078.
- Lopez, A.S, Belloso, O.M. (2008). Use of nisin and other bacteriocins for preservation of production in a Lactobacillus rn78 strain isolated from a dairy sample in Iran. Med. J. Islamic World Acad. Sci., 16 (1): 19-24, doi.org/10.1016/j.idairyj.2007.11.009.
- Mayr-Harting, A. (1972). Methods for studying bacteriocins. Meth. Microbiol., 7: 315-422.
- Moreno, M.R., Leisner, J.J., Tee, L.K, Ley, C., Radu, S., Rusul, G., Vancanneyt, M., De Vuyst, L. (2002). Microbial analysis of malaysian tempeh, and characterization of two bacteriocins produced by isolates of Enterococcus faecium. J. Appl. Microbiol., 92 (1): 147-157, https://doi.org/10.1046/j.1365-2672.2002.01509.x
- Moreno, Y., Collado, M.C., Ferrus, M.A., Cobo, J.M., Hernandez, E., Hernandez, M. (2006). Viability assessment of lactic acid bacteria in commercial dairy products stored at 4 °C using LIVE/DEAD® BacLight™ staining and conventional plate counts. J. Food Sci. Technol., 41: 275-280, doi.org/10.1111/j.1365-2621.2005.01060.x
- Öncül, N., Yıldırım, Z. Yıldırım, M. (2015). Laktokoksiz BZ ve Enterosin KP’nin Yoğurt Kültürlerinin Aktivitesi Üzerine Etkisi. TURJAF, 3(5): 342-345.
- O'Sullivan, L., Ross, R.P., Hill, C. (2002). Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie, 84: 593-604, doi.org/10.1016/S0300-9084(02)01457-8
- Papagianni, M. (2003). Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnol. Adv., 21: 465-499, doi.org/10.1016/S0734-9750(03)00077-6.
- Penna, T.C.V., Jozala, A.F., Novaes, L.C.L., Pessoa, A., Cholewa, O. (2005). Production of nisin by Lactococcus lactis in media with skimmed milk. Biotechnol. Appl. Biochem., 122: 619-637, doi.org/10.1385/ABAB:122:1-3:0619
- Rodriguez, J.M., Martinez, M.I., Horn, N., Dodd, H.M. (2003). Heterologous production of bacteriocins by lactic acid bacteria. Int. J. Food Microbiol., 80: 101-116, doi.org/10.1016/S0168-1605(02)00153-8.
- Rodriıguez, E., Calzadaa J., Arque, J.L., Rodrıguez, J.M, Nuneza, M., Medinaa, M. (2005). Antimicrobial activity of pediocin-producing Lactococcus lactis on Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 in cheese. Int. Dairy J., 15: 51-57, doi.org/10.1016/j.idairyj.2004.05.004.
- Şahingil, D., İşleroğlu, H., Yıldırım, Z., Akçelik, M., Yıldırım, M. (2011). Characterization of lactococcin BZ produced by Lactococcus lactis subsp. lactis BZ isolated from boza. Turk. J. Biol., 35(1): 21-33, doi:10.3906/biy-0906-48
- Simova, E.D., Beshkova, Angelov, D.M., Dimitrov, M.P.P. (2008). Bacteriocin production by strain Lactobacillus delbrueckii ssp. bulgaricus BB18 during continuous prefermentation of yogurt starter culture and subsequent batch coagulation of milk. J. Microbiol. Biotechnol., 35: 559-567, DOI 10.1007/s10295-008-0317-x.
- Soomro, A.H., Masud, T., Anwaar, K. (2002). Role of lactic acid bacteria (LAB) in food preservation and human health – A Review. Pak. J. Nutr., 1(1): 20-24.
- Wan, J., Harmark, K., Davidson, B.E., Hillier, A.J., Gordon, J.B., Wilcock, A., Hickey, M.W., Coventry, M.J. (1997). Inhibition of Listeria monocytogenes by piscicolin 126 in milk and Camembert cheese manufactured with a thermophilic starter. J. Appl. Microbiol. 28: 273-280, doi.org/10.1046/j.1365-2672.1997.00349.x
BAKTERİYOSİNOJENİK SUŞLARIN SÜTTE GELİŞMELERİ VE BAKTERİYOSİNLERİNİN PEYNİR KÜLTÜRLERİNE KARŞI AKTİVİTELERİ
Year 2020,
Volume: 45 Issue: 6, 1175 - 1187, 12.10.2020
Nilgün Öncül
,
Zeliha Yıldırım
Abstract
Bu çalışmada; farklı yağ içeriğine sahip sütlerde bakteriyosin üreticisi olan Lactococcus lactis ssp. lactis BZ ve Enterococcus faecalis KP’nin gelişme ve bakteriyosin üretme yetenekleri ile bakteriyosinleri olan laktokoksin BZ ve enterosin KP’nin tam yağlı sütte peynir üretiminde kullanılan starter kültürlere (Choozit MA 11LYO 50, Choozit MA 19LYO 50 ve DI-Prox M265) karşı etkileri belirlenmiştir. L. lactis ssp. lactis BZ ve E. faecalis KP’nin sütte gelişme ve bakteriyosin üretme yetenekleri 30°C’de 48 saat boyunca incelenmiştir. Çalışma sonucunda, her iki bakterinin düşük yağ içeriğine sahip sütte daha iyi geliştikleri ve daha fazla bakteriyosin ürettikleri tespit edilmiştir. Laktokoksin BZ (1600 AU/mL) ve enterosin KP (1600 AU/mL) hem tek başlarına hem de kombine olarak kullanıldıklarında analiz edilen üç farklı peynir starter kültürlerine karşı inhibitör etkinliğe sahip olduğu bulunmuştur.
References
- Aasen, I.M., Moreto, T., Katla, T. (2000). Influence of complex nutrients, temperature and pH on bacteriocins production by Lactobacillus sakei CCUG 42687. Appl. Microbiol. Biotechnol 53: 159-166.
- AOAC (1995). Official methods of analysis of AOAC INTERNATIONAL, 16th Edition, Washington, D.C., the USA.
- Ávila, M., Gómez‐Torres, N., Gaya, P., Garde, S. (2020). Effect of a nisin‐producing lactococcal starter on the late blowing defect of cheese caused by Clostridium tyrobutyricum. Int J Food Scı Tech 1-7, doi.org/10.1111/ijfs.14598.
- Beasley, S. (2004). Isolation, identification and exploitation lactic acid bacteria from human and animal microbiota. University of Helsinki, Faculty of Agriculture and Forestry and Viikki Graduate School in Biosciences, Department of Applied Chemistry and Microbiology Division of Microbiology, Academic Dissertation, Helsinki, Finland, 57 pages.
- Benmouna1, Z., Dalache, F., Karam, N., Zadi-Karam, H. (2018). Optimization and some characteristics of bacteriocin produced by Enterococcus sp. CM9 collected from Mauritanian Camel milk. Emir J Food Agr 30(4): 275-282, DOI https://doi.org/10.9755/ejfa.2018.v30.i4.1662.
- Bizani, D., Morrissy, J.A.C., Dominguez, A.P.M., Brandelli, A. (2008). Inhibition of Listeria monocytogenes in dairy products using the bacteriocin-like peptide cerein 8A. Int. J. Food Microbiol., 121 (2): 229–233, doi.org/10.1016/j.ijfoodmicro.2007.11.016.
- Chen, H., Hoover, D.G. (2003). Bacteriocins and their food applications. Compr. Rev. Food Sci. Food Saf. 2: 82-100, doi.org/10.1111/j.1541-4337.2003.tb00016.x.
- Cintas, L.M., Casaus, M.P., Herranz, C., Nes, I.F., Hernández, P.E. (2001). Review: bacteriocins of lactic acid bacteria. Food Sci Technol Int, 7 (4): 281-305, doi.org/10.1106/R8DE-P6HU-CLXP-5RYT.
- Cleveland, J., Montville, T.J., Nes, I.F., Chikindas, M.L. (2001). Bacteriocins: safe, natural antimicrobials for food preservation. Int. J. Food Microbiol., 71, 1-20, doi.org/10.1016/S0168-1605(01)00560-8.
- De Vuyst, L., Leroy, F. (2007). Bacteriocins from lactic acid bacteria: production, purification, and food application. J Mol Microbiol Biotechnol, 13: 194-199, doi.org/10.1159/000104752.
- Deegan, L.H., Cotter, P.D., Hill, C., Ross, P. (2006). Bacteriocins: biological tools for biopreservation and shelf-life extension. Int. Dairy J. 16: 1058–1071, doi.org/10.1016/j.idairyj.2005.10.026.
- Eissa, S. A., Elbarbary, H. A., Ibrahim, E., & Mohammed, H. A. (2018). Growth pattern of starter cultures and antifungal activity of some bacteriocins and ınulin in skim milk yoghurt. Alex. J. Vet. Sci., 59 (2): 17-25, DOI: 10.5455/ajvs.12522
- Foulquie Moreno, M.R., Callewaert, R., Devreese, B., Beeumen, J.V., De Vuyst, L. (2003). Isolation and biochemical characterisation of enterocins produced by enterococci from different sources. J. Appl. Microbiol, 94: 214-229.
- Galvez, A., Abriouel, H., Lopez, R.L., Omar, N.B. (2007). Bacteriocin-based strategies for food biopreservation. Int. J. Food Microbiol., 120: 51-70.
- Garde, S., Ávila, M., Arias, R., Gaya, P., Nuñez, M. (2011). Outgrowth inhibition of Clostridium beijerinckii spores by a bacteriocin-producing lactic culture in ovine milk cheese. Int. J. Food Microbiol., 150: 59–65.
- Isleroglu, H., Yildirim, Z., Tokatli, M., Oncul, N., Yildirim, M. (2012). Partial characterisation of enterocin KP produced by Enterococcus faecalis KP, a cheese isolate. Int. J. Dairy Technol., 65: 90-97.
- Khalid, F., Siddiqi, R., Mojgani, N. (1999). Detection and characterization of a heat stable bacteriocin (lactocin Lc-09) produced by a clinical isolate of lactobacilli. Med. J. İslamic World Acad. Sci. 12 (3): 67-71.
- Klaenhammer, T.R. (1993). Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Lett., 12: 39-86, doi.org/10.1111/j.1574-6976.1993.tb00012.x
- Kuipers, O.P.P., Ruyter, G.G., Kleerebezem, A.M., Vos, W.M. (1997). Controlled overproduction of proteins by lactic acid bacteria. Trends Biotechnol., 15: 135-140, doi.org/10.1016/S0167-7799(97)01029-9.
- Lacrois, I.C. (2008). Cheese cultures: From just acidification to complex functionalities. 5th DF Symposium on Cheese Ripening, 9-13 March, 2008, Bern, Switzeland.
- Lauková, A., Czikková, S. (2001). Antagonistic effect of enterocin CCM 4231 from Enterococcus faecium on “bryndza”, a traditional Slovak dairy product from sheep milk. Microbiol. Res, 156: 31- 34, doi.org/10.1078/0944-5013-00078.
- Lopez, A.S, Belloso, O.M. (2008). Use of nisin and other bacteriocins for preservation of production in a Lactobacillus rn78 strain isolated from a dairy sample in Iran. Med. J. Islamic World Acad. Sci., 16 (1): 19-24, doi.org/10.1016/j.idairyj.2007.11.009.
- Mayr-Harting, A. (1972). Methods for studying bacteriocins. Meth. Microbiol., 7: 315-422.
- Moreno, M.R., Leisner, J.J., Tee, L.K, Ley, C., Radu, S., Rusul, G., Vancanneyt, M., De Vuyst, L. (2002). Microbial analysis of malaysian tempeh, and characterization of two bacteriocins produced by isolates of Enterococcus faecium. J. Appl. Microbiol., 92 (1): 147-157, https://doi.org/10.1046/j.1365-2672.2002.01509.x
- Moreno, Y., Collado, M.C., Ferrus, M.A., Cobo, J.M., Hernandez, E., Hernandez, M. (2006). Viability assessment of lactic acid bacteria in commercial dairy products stored at 4 °C using LIVE/DEAD® BacLight™ staining and conventional plate counts. J. Food Sci. Technol., 41: 275-280, doi.org/10.1111/j.1365-2621.2005.01060.x
- Öncül, N., Yıldırım, Z. Yıldırım, M. (2015). Laktokoksiz BZ ve Enterosin KP’nin Yoğurt Kültürlerinin Aktivitesi Üzerine Etkisi. TURJAF, 3(5): 342-345.
- O'Sullivan, L., Ross, R.P., Hill, C. (2002). Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie, 84: 593-604, doi.org/10.1016/S0300-9084(02)01457-8
- Papagianni, M. (2003). Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnol. Adv., 21: 465-499, doi.org/10.1016/S0734-9750(03)00077-6.
- Penna, T.C.V., Jozala, A.F., Novaes, L.C.L., Pessoa, A., Cholewa, O. (2005). Production of nisin by Lactococcus lactis in media with skimmed milk. Biotechnol. Appl. Biochem., 122: 619-637, doi.org/10.1385/ABAB:122:1-3:0619
- Rodriguez, J.M., Martinez, M.I., Horn, N., Dodd, H.M. (2003). Heterologous production of bacteriocins by lactic acid bacteria. Int. J. Food Microbiol., 80: 101-116, doi.org/10.1016/S0168-1605(02)00153-8.
- Rodriıguez, E., Calzadaa J., Arque, J.L., Rodrıguez, J.M, Nuneza, M., Medinaa, M. (2005). Antimicrobial activity of pediocin-producing Lactococcus lactis on Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 in cheese. Int. Dairy J., 15: 51-57, doi.org/10.1016/j.idairyj.2004.05.004.
- Şahingil, D., İşleroğlu, H., Yıldırım, Z., Akçelik, M., Yıldırım, M. (2011). Characterization of lactococcin BZ produced by Lactococcus lactis subsp. lactis BZ isolated from boza. Turk. J. Biol., 35(1): 21-33, doi:10.3906/biy-0906-48
- Simova, E.D., Beshkova, Angelov, D.M., Dimitrov, M.P.P. (2008). Bacteriocin production by strain Lactobacillus delbrueckii ssp. bulgaricus BB18 during continuous prefermentation of yogurt starter culture and subsequent batch coagulation of milk. J. Microbiol. Biotechnol., 35: 559-567, DOI 10.1007/s10295-008-0317-x.
- Soomro, A.H., Masud, T., Anwaar, K. (2002). Role of lactic acid bacteria (LAB) in food preservation and human health – A Review. Pak. J. Nutr., 1(1): 20-24.
- Wan, J., Harmark, K., Davidson, B.E., Hillier, A.J., Gordon, J.B., Wilcock, A., Hickey, M.W., Coventry, M.J. (1997). Inhibition of Listeria monocytogenes by piscicolin 126 in milk and Camembert cheese manufactured with a thermophilic starter. J. Appl. Microbiol. 28: 273-280, doi.org/10.1046/j.1365-2672.1997.00349.x