Abstract
Bacteriocins are being used as new food biopreservative agents. In general, bacteriocins produced by Gram-positive bacteria are active against other Gram-positive. Basically, the same principle applies to those produced by Gram-negative bacteria. They have a restricted spectrum of action against related bacteria to those that produce the bacteriocin. Therefore, other hurdles or chemical preservatives are necessary to apply to broaden the spectrum of action of bacteriocins in foods. This is a further and deeper study of the possible application of the hybrid wide-spectrum bacteriocin named Ent35-MccV in food. Its antimicrobial activity was assayed in skim milk and patties as food models against Listeria monocytogenes and Escherichia coli. The influence of the temperature and digestive proteases on its biological activity and its antimicrobial activity was tested in vitro on a variety of pathogenic and food spoilage bacteria. The results showed that Ent35-MccV could inhibit the growth of both the Gram-positive L. monocytogenes and the Gram-negative E. coli in model food, and its activity was not affected by heating conditions including autoclaving. E. coli strains and Listeria spp. are the most affected bacteria, but Ent35-MccV showed antimicrobial activity against some strain of Salmonella spp., Staphylococcus epidermidis, Enterobacter aerogenes, Morganella morgani, Proteus mirabilis, Shigella boydii, Shigella flexneri, and Shigella sonnei.
Similar content being viewed by others
References
Acuña, L., Morero, R., & Bellomio, A. (2011). Development of wide-spectrum hybrid bacteriocins for food biopreservation. Food and Bioprocess Technology, 4(6), 1029–1049. doi:10.1007/s11947-010-0465-7.
Acuña, L., Picariello, G., Sesma, F., Morero, R. D., & Bellomio, A. (2012). A new hybrid bacteriocin, Ent35–MccV, displays antimicrobial activity against pathogenic Gram-positive and Gram-negative bacteria. FEBS Open Bio, 2, 12–19. doi:10.1016/j.fob.2012.01.002.
Benmechernene, Z., Fernandez-No, I., Kihal, M., Böhme, K., Calo-Mata, P., & Barros-Velazquez, J. (2013). Recent patents on bacteriocins: food and biomedical applications. Recent patents on DNA & gene sequences, 7(1), 66–73.
Calo-Mata, P., Arlindo, S., Boehme, K., de Miguel, T., Pascoal, A., & Barros-Velazquez, J. (2008). Current applications and future trends of lactic acid bacteria and their bacteriocins for the biopreservation of aquatic food products. Food and Bioprocess Technology, 1(1), 43–63. doi:10.1007/s11947-007-0021-2.
Castellano, P., Belfiore, C., & Vignolo, G. (2011). Combination of bioprotective cultures with EDTA to reduce Escherichia coli O157:H7 in frozen ground-beef patties. Food Control, 22(8), 1461–1465. doi:10.1016/j.foodcont.2011.02.018.
Chalón, M. C., Acuña, L., Morero, R. D., Minahk, C. J., & Bellomio, A. (2012). Membrane-active bacteriocins to control Salmonella in foods: are they the definite hurdle? Food Research International, 45(2), 735–744. doi:10.1016/j.foodres.2011.08.024.
Chen, C. M., Sebranek, J. G., Dickson, J. S., & Mendonca, A. F. (2004). Combining pediocin with postpackaging irradiation for control of Listeria monocytogenes on frankfurters. Journal of Food Protection, 67(9), 1866–1875.
Chi-Zhang, Y., Yam, K. L., & Chikindas, M. L. (2004). Effective control of Listeria monocytogenes by combination of nisin formulated and slowly released into a broth system. International Journal of Food Microbiology, 90(1), 15–22.
Chounou, N., Chouliara, E., Mexis, S. F., Stavros, K., Georgantelis, D., & Kontominas, M. G. (2013). Shelf life extension of ground meat stored at 4 °C using chitosan and an oxygen absorber. International Journal of Food Science and Technology, 48(1), 89–95.
Cintas, L. M., Casaus, P., Håvarstein, L. S., Hernández, P. E., & Nes, I. F. (1997). Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum. Applied and Environmental Microbiology, 63(11), 4321–4330. Accessed 22 June 2010.
Cleveland, J., Montville, T. J., Nes, I. F., & Chikindas, M. L. (2001). Bacteriocins: safe, natural antimicrobials for food preservation. International Journal of Food Microbiology, 71(1), 1–20. Accessed 25 January 2011.
Concha, R., Farías, M. E., Kümmerlin, R., & Sesma, F. (1999). Enterocin-35, a bacteriocin with activity against Listeria monocytogenes. Possible use in the food industry. Revista Latinoamericana de Microbiología, 41(3), 133–138.
Cotter, P. D., Hill, C., & Ross, R. P. (2005). Bacteriocins: developing innate immunity for food. Nature reviews. Microbiology, 3(10), 777–788. doi:10.1038/nrmicro1273.
Delmore, J.R. (2009). Beef Shelf-life. http://www.beefresearch.org/cmdocs/beefresearch/pe/beef_shelf_life.pdf. Accessed 15 Dec 2014.
Duquesne, S., Destoumieux-Garzón, D., Peduzzi, J., & Rebuffat, S. (2007). Microcins, gene-encoded antibacterial peptides from enterobacteria. Natural Product Reports, 24(4), 708–734. doi:10.1039/b516237h.
Farias, M. E., De Ruiz Holgado, A. A. P., & Sesma, F. (1994). Bacteriocin production by lactic acid bacteria isolated from regional cheeses: inhibition of foodborne pathogens. Journal of Food Protection, 57(11), 1013–1015.
Fath, M. J., Zhang, L. H., Rush, J., & Kolter, R. (1994). Purification and characterization of colicin V from Escherichia coli culture supernatants. Biochemistry, 33(22), 6911–6917.
Fernández-No, I. C., Böhme, K., Gallardo, J. M., Barros-Velázquez, J., Cañas, B., & Calo-Mata, P. (2010). Differential characterization of biogenic amine-producing bacteria involved in food poisoning using MALDI-TOF mass fingerprinting. Electrophoresis, 31(6), 1116–1127. doi:10.1002/elps.200900591.
Gao, Y., Li, D., & Liu, X. (2013). Evaluation of the factors affecting the activity of sakacin C2 against E. coli in milk. Food Control, 30(2), 453–458. doi:10.1016/j.foodcont.2012.07.013.
Giraffa, G., Neviani, E., & Tarelli, G. T. (1994). Antilisterial activity by enterococci in a model predicting the temperature evolution of Taleggio, an Italian soft cheese. Journal of Dairy Science, 77(5), 1176–1182. doi:10.3168/jds.S0022-0302(94)77055-7.
Hammami, R., Zouhir, A., Le Lay, C., Ben Hamida, J., & Fliss, I. (2010). BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiology, 10, 22. doi:10.1186/1471-2180-10-22.
Huq, T., Vu, K. D., Riedl, B., Bouchard, J., & Lacroix, M. (2015). Synergistic effect of gamma (γ)-irradiation and microencapsulated antimicrobials against Listeria monocytogenes on ready-to-eat (RTE) meat. Food Microbiology, 46, 507–514. doi:10.1016/j.fm.2014.09.013.
Jin, T., Liu, L., Sommers, C. H., Boyd, G., & Zhang, H. (2009). Radiation sensitization and post irradiation proliferation of Listeria monocytogenes on ready-to-eat deli meat in the presence of pectin-nisin films. Journal of Food Protection, 72(3), 644–649.
Juneja, V. K., Altuntaş, E. G., Ayhan, K., Hwang, C.-A., Sheen, S., & Friedman, M. (2013). Predictive model for the reduction of heat resistance of Listeria monocytogenes in ground beef by the combined effect of sodium chloride and apple polyphenols. International Journal of Food Microbiology, 164(1), 54–59. doi:10.1016/j.ijfoodmicro.2013.03.008.
Leistner, L. (1978). Hurdle effect and energy saving. In W. K. Downey (Ed.), Food quality and nutrition (pp. 553–557). London: Applied Science Publishers.
Leistner, L., & Grahame, W. (2005). Update on hurdle technology approaches to food preservation. In P. M. Davidson, J. N. Sofos, & A. L. Branen (Eds.), Antimicrobials in Food, Third Edition (3rd ed., pp. 621–641). CRC Press.
Li, D., Liu, X., & Gao, Y. (2014). Synergistic Effects of sakacin C2 in combination with food preservatives. In T.-C. Zhang, P. Ouyang, S. Kaplan, & B. Skarnes (Eds.), Proceedings of the 2012 International Conference on Applied Biotechnology (ICAB 2012) (pp. 455–464). Springer Berlin Heidelberg. http://link.springer.com/chapter/10.1007/978-3-642-37916-1_47.
Metaxopoulos, J., Mataragas, M., & Drosinos, E. H. (2002). Microbial interaction in cooked cured meat products under vacuum or modified atmosphere at 4 degrees C. Journal of Applied Microbiology, 93(3), 363–373.
Minahk, C. J., Saavedra, L., Sesma, F., & Morero, R. (2005). Membrane viscosity is a major modulating factor of the enterocin CRL35 activity. Biochimie, 87(2), 181–186. doi:10.1016/j.biochi.2004.10.013.
Miranda, J. M., Vázquez, B. I., Fente, C. A., Calo-Mata, P., Cepeda, A., & Franco, C. M. (2008). Comparison of antimicrobial resistance in Escherichia coli, Staphylococcus aureus, and Listeria monocytogenes strains isolated from organic and conventional poultry meat. Journal of Food Protection, 71(12), 2537–2542.
Mitra, S., Mukhopadhyay, B. C., & Biswas, S. R. (2011). Potential application of the nisin Z preparation of Lactococcus lactis W8 in preservation of milk. Letters in Applied Microbiology, 53(1), 98–105. doi:10.1111/j.1472-765X.2011.03075.x.
Morgan, S. M., Galvin, M., Kelly, J., Ross, R. P., & Hill, C. (1999). Development of a lacticin 3147-enriched whey powder with inhibitory activity against foodborne pathogens. Journal of Food Protection, 62(9), 1011–1016.
Murdock, C. A., Cleveland, J., Matthews, K. R., & Chikindas, M. L. (2007). The synergistic effect of nisin and lactoferrin on the inhibition of Listeria monocytogenes and Escherichia coli O157:H7. Letters in Applied Microbiology, 44(3), 255–261. doi:10.1111/j.1472-765X.2006.02076.x.
Nielsen, J. W., Dickson, J. S., & Crouse, J. D. (1990). Use of a bacteriocin produced by Pediococcus acidilactici to inhibit Listeria monocytogenes associated with fresh meat. Applied and Environmental Microbiology, 56(7), 2142–2145. Accessed 2 June 2014.
Pomares, M. F., Salomón, R. A., Pavlova, O., Severinov, K., Farías, R., & Vincent, P. A. (2009). Potential applicability of chymotrypsin-susceptible microcin J25 derivatives to food preservation. Applied and Environmental Microbiology, 75(17), 5734–5738. doi:10.1128/AEM. 01070-09.
Pucci, M. J., Vedamuthu, E. R., Kunka, B. S., & Vandenbergh, P. A. (1988). Inhibition of Listeria monocytogenes by using bacteriocin PA-1 produced by Pediococcus acidilactici PAC 1.0. Applied and Environmental Microbiology, 54(10), 2349–2353.
Ray, B., & Bhunia, A. (2007). Fundamental Food Microbiology, Fourth Edition (4th ed.). CRC Press.
Rørvik, L. M. (2000). Listeria monocytogenes in the smoked salmon industry. International Journal of Food Microbiology, 62(3), 183–190.
Ryan, M. P., Rea, M. C., Hill, C., & Ross, R. P. (1996). An application in cheddar cheese manufacture for a strain of Lactococcus lactis producing a novel broad-spectrum bacteriocin, lacticin 3147. Applied and Environmental Microbiology, 62(2), 612–619.
Saavedra, L., Minahk, C., de Ruiz Holgado, A. P., & Sesma, F. (2004). Enhancement of the enterocin CRL35 activity by a synthetic peptide derived from the NH2-terminal sequence. Antimicrobial Agents and Chemotherapy, 48(7), 2778–2781. doi:10.1128/AAC. 48.7.2778-2781.2004.
Saavedra, L., Bellomio, A., Hebert, E., Minahk, C. J., Suarez, N., & Sesma, F. (2012). Listeria: epidemiology, pathogenesis and novel potential treatments. In applications of natural products in food. Nueva York: Nova Science Publishers.
Salomón, R. A., & Farías, R. N. (1992). Microcin 25, a novel antimicrobial peptide produced by Escherichia coli. Journal of Bacteriology, 174(22), 7428–7435.
Sánchez-Hidalgo, M., Montalbán-López, M., Cebrián, R., Valdivia, E., Martínez-Bueno, M., & Maqueda, M. (2011). AS-48 bacteriocin: close to perfection. Cellular and Molecular Life Sciences: CMLS, 68(17), 2845–2857. doi:10.1007/s00018-011-0724-4.
Schillinger, U., Chung, H. S., Keppler, K., & Holzapfel, W. H. (1998). Use of bacteriocinogenic lactic acid bacteria to inhibit spontaneous nisin-resistant mutants of Listeria monocytogenes Scott A. Journal of Applied Microbiology, 85(4), 657–663.
Schmidt, S. E., Holub, G., Sturino, J. M., & Taylor, T. M. (2009). Suppression of Listeria monocytogenes Scott A in fluid milk by free and liposome-entrapped nisin. Probiotics and Antimicrobial Proteins, 1(2), 152–158. doi:10.1007/s12602-009-9022-y.
Smigic, N., & Rajkovic, A. (2014). Hurdle technology. In V. R. Rai & J. A. Bai (Eds.), Microbial food safety and preservation techniques (1st ed.). Boca Raton: CRC Press.
Sobrino-López, A., & Martín-Belloso, O. (2008). Use of nisin and other bacteriocins for preservation of dairy products. International Dairy Journal, 18(4), 329–343. doi:10.1016/j.idairyj.2007.11.009.
Techathuvanan, C., Reyes, F., David, J. R. D., & Davidson, P. M. (2014). Efficacy of commercial natural antimicrobials alone and in combinations against pathogenic and spoilage microorganisms. Journal of Food Protection, 77(2), 269–275. doi:10.4315/0362-028X.JFP-13-288.
Turner, M. (2011). Microbe outbreak panics Europe. Nature News, 474(7350), 137–137. doi:10.1038/474137a.
Uesugi, A. R., & Moraru, C. I. (2009). Reduction of Listeria on ready-to-eat sausages after exposure to a combination of pulsed light and nisin. Journal of Food Protection, 72(2), 347–353.
Vignolo, G., Palacios, J., Farias, M. E., Sesma, F., Schillinger, U., Holzapfel, W., & Oliver, G. (2000). Combined effect of bacteriocins on the survival of various Listeria species in broth and meat system. Current Microbiology, 41(6), 410–416.
WHO. (2011). A Public Health Review of the enterohaemorrhagic Escherichia coli outbreak in Germany. http://www.euro.who.int/en/health-topics/disease-prevention/food-safety/publications/2011/a-public-health-review-of-the-enterohaemorrhagic-escherichia-coli-outbreak-in-germany. Accessed 25 Feb 2014.
WHO/FAO. (n.d.). CODEX Alimentarius: Standards. http://www.codexalimentarius.org/standards/en/. Accessed 4 Apr 2014.
Wulijideligen, N., Asahina, T., Hara, K., Arakawa, K., Nakano, H., & Miyamoto, T. (2012). Production of bacteriocin by Leuconostoc mesenteroides 406 isolated from Mongolian fermented mare’s milk, airag. Animal Science Journal, 83(10), 704–711. doi:10.1111/j.1740-0929.2012.01010.x.
Acknowledgments
Financial support was provided by Grants PIP 0779 from CONICET, PICT 2998 from the Agencia Nacional de Promoción Científica y Tecnológica ANPCyT, and PIUNT D548/1 from UNT. This work was also funded by the project 10PXIB261045PR from Xunta de Galicia and by the project AGL2010-19646 from the Spanish Ministry of Science and Technology. The work of L. Acuña is supported by CONICET and USC-Santander fellowships. N. Corbalan is recipient of a CONICET fellowship. The work of I.C. Fernandez was supported by a “Lucas Labrada” research contract from Xunta de Galicia. The authors thank Carlos Franco and José M. Miranda for providing generously the E. coli, Salmonella spp., and L. monocytogenes food isolates.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Acuña, L., Corbalan, N.S., Fernandez-No, I.C. et al. Inhibitory Effect of the Hybrid Bacteriocin Ent35-MccV on the Growth of Escherichia coli and Listeria monocytogenes in Model and Food Systems. Food Bioprocess Technol 8, 1063–1075 (2015). https://doi.org/10.1007/s11947-015-1469-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-015-1469-0