Synergistic Effect of Enterocin NKR-5-3 and Sodium Citrate against Listeria innocua ATCC 33090 in Culture Media and Chilled Shrimp
Main Article Content
Abstract
Enterocin NKR-5-3, an antimicrobial peptide and class II bacteriocin, is produced by Enterococcus faecium NKR-5-3 isolated from Thai fermented fish. However, it displays low antimicrobial activity against Listeria spp., which are recognized as significant food-borne bacteria in seafood industries. In this study, commercial food additives with potential ability to enhance bacteriocin activity, including ethylenediaminetetraacetic acid (EDTA), sodium lactate (SL), and sodium citrate (SC), were applied to enhance antimicrobial activity of enterocin NKR-5-3 against L. innocua ATCC 33090. The results showed that only 1.5% (w/v) SC could produce a significantly more effective (p<0.05) synergistic interaction with enterocin NKR-5-3 against L. innocua ATCC 33090 when comparing with EDTA (250 ppm) and SL (2% v/v). The combination of enterocin NKR-5-3 at final concentration of 3,200 AU·mL-1 and 1.5% (w/v) SC could reduce the count of L. innocua ATCC 33090 by 1.33, 1.14, 0.97 and 1.13 log CFU·mL-1 in culture broth at 4 °C after 16 h of incubation period, when compared to the control, treatment with only SC, treatment with only enterocin NKR-5-3, and initial loading number, respectively. The synergistic interaction of enterocin NKR-5-3 and SC enhanced the bactericidal mode of action against L. innocua ATCC 33090, confirmed by total viable count in culture media together with morphological damage of target cells observed by SEM. In artificially contaminated shrimp meat samples kept at 4 °C for 48 h, the combination of enterocin NKR-5-3 and SC could reduce the count of L. innocua ATCC 33090 by 1.89, 1.78, 1.30 and 0.81 log CFU·g-1 compared to the control, treatment with only SC, only enterocin NKR-5-3, and initial loading number, respectively.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Abriouel, H., E. Valdivia, A. Galvez and M. Maqueda. 1998. Response of Salmonella Choleraesuis LT2 spheroplasts and permeabilized cells to the bacteriocin AS-48. Applied and Environmental Microbiology 64: 4623-4626.
Aichinger, E. 2010. Listeria infections in Baden-Württemberg and Bavaria, October-November 2010. Epidemiological Bulletin 47: 463-471.
Alakomi, H.L., E. Skyttä, M. Saarela, T.M. Sandholm, K.L. Kala and I.M. Helander. 2000. Lactic acid permeabilizes Gram-negative bacteria by disrupting the outer membrane. Applied and Environmental Microbiology 66(5): 2001-2005.
Ananou, S., A. Ga´lvez, M. Martı´nez-Bueno, M. Maqueda and E. Valdivi. 2005. Synergistic effect of enterocin AS-48 in combination with outer membrane permeabilizing treatments against Escherichia coli O157:H7. Journal of Applied Microbiology 99: 1364-1372.
Ayres, H.M., J.R. Furr and A.D. Ruseel. 1999. Effect of divalent cations on permeabilizer-induced lysozyme lysis of Pseudomonas aeruginosa. Letters in Applied Microbiology 27: 372-374.
Bari, M.L., D.O. Ukuku, T. Kawasaki, Y. Inatsu, K. Isshiki and S. Kawamoto. 2005. Combined efficacy of nisin and pediocin with sodium lactate, citric acid, phytic acid, and potassium sorbate and EDTA in reducing the Listeria monocytogenes population of inoculated fresh-cut produce. Journal of Food Protection 68(7): 1381-1387.
Belfiore, C., P. Castellano and G. Vignolo. 2007. Reduction of Escherichia coli population following treatment with bacteriocins from lactic acid bacteria and chelators. Food Microbiology 24: 223-229.
Buchanan, R.L., L.G.M. Gorris, M.M. Hayman, T.C. Jackson and R.C. Whiting. 2017. A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control 75: 1-13.
Buncic, S., S. Fitzgerald, C.M. Bell and R.G. Hudson. 1995. Individual and combined listericidal effects of sodium lactate, potassium sorbate, nisin and curing salts at refrigeration temperatures. Journal of Food Safety 15: 247-264.
Centers for Disease Control and Prevention. 2022. Listeria (Listeriosis). https://www.cdc.gov/listeria/. Cited 1 Jul 2022.
Cleveland, J., T.J. Montville, I.F. Nes and M.L. Chikindas. 2001. Bacteriocins: safe, natural antimicrobial for food preservation. International Journal of Food Microbiology 71: 1-20.
Costa, A., A. Lourenco, T. Civera and L. Brito. 2018. Listeria innocua and Listeria monocytogenes strains from dairy plants behave similarly in biofilm sanitizer testing. LWT-Food Science and Technology 92: 477-483.
De Vuyst, L. and E.J. Vandamme. 1994. Antimicrobial potential of lactic acid bacteria. In: Bacteriocins of Lactic Acid Bacteria: Microbiology, Genetic and Application (eds. L. De Vuyst and E.J. Vandamme), pp. 91-142. Blackie Academic and Professional, London, UK.
Doores, S. 1993. Organic acids. In: Antimicrobials in Foods (eds. P.M. Davidson and A.L. Branen), pp. 95-136. Marcel Dekker, Inc., New York, USA.
Du, H., J. Yang, X. Lu, Z. Lu, X. Bie, H. Zhao, C. Zhang and F. Lu. 2018. Purification, characterization, and mode of action of plantaricin GZ1-27, a novel bacteriocin against Bacillus cereus. Journal of Agricultural and Food Chemistry 66(18): 4716-4724.
Elson, R., A. Awofisayo-Okuyelu, T. Greener, C. Swift, A. Painset, C.F.L. Amar, A. Newton, H. Aird, M. Swindlehurst, N. Elviss, K. Foster, T.J. Dallman, R. Ruggles and K. Grant. 2019. Utility of whole genome sequencing to describe the persistence and evolution of Listeria monocytogenes strains within crabmeat processing environments linked to two outbreaks of listeriosis. Journal of Food Protection 82: 30-38.
Ennahar, S., T. Sashihara, K. Sonomoto and A. Ishizaki. 2000. Class II a bacteriocins: biosynthesis, structure and activity. FEMS Microbiology Reviews 24: 85-106.
European Centre for Disease Prevention and Control and European Food Safety Authority. 2019. Multi-country outbreak of Listeria monocytogenes clonal complex 8 infections linked to consumption of cold-smoked fish products. https://efsa.onlinelibrary.wiley.com/doi/abs/10.2903/sp.efsa.2019.EN-1665. Cited 2 Aug 2022.
European Food Safety Authority and European Centre for Disease Prevention and Control. 2021. The European Union One Health 2020 Zoonoses Report. https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/j.efsa.2021.6971. Cited 2 Aug 2022.
Freitag, N.E., G.C. Port and M.D. Miner. 2009. Listeria monocytogenes-from saprophyte to intracellular pathogen. Nature Reviews Microbiology 7: 623-628.
Ganzle, M.G., S. Weber and W.P. Hammes. 1999. Effect of ecological factors on the inhibitory spectrum and activity of bacteriocins. International Journal of Food Microbiology 46: 207-217.
Gao, Y., M.J. Van Belkum and M.E. Stiles. 1999. The outer membrane of Gram-negative bacteria inhibits antibacterial activity of Brochocin-C. Applied and Environmental Microbiology 65: 4329-4333.
Giraffa, G., D. Carminati and G.T. Tarelli. 1995. Inhibition of Listeria innocua in milk by bacteriocin-producing Enterococcus faecium 7C5. Journal of Food Protection 58(6): 621-623.
Grande, M.J., R. Lucas, H. Abriouel, E. Valdivia, N. Ben Omar, M. Maqueda, M. Martínez-Bueno, M. Martínez-Cañamero and A. Gálvez. 2006. Inhibition of toxicogenic Bacillus cereus in rice-based foods by enterocin AS-48. International Journal of Food Microbiology 106: 185-194.
He, Y., X. Zhao, L. Chen, L. Zhao and H. Yang. 2021. Effect of electrolysed water generated by sodium chloride combined with sodium bicarbonate solution against Listeria innocua in broth and on shrimp. Food Control 127: 108134. DOI: 10.1016/j.foodcont.2021.108134.
Ishibashi, N., N. Matsumoto, R.H. Perez, S. Iwatani, H. Sugino, T. Zendo, P. Wilaipun, V. Leelawatcharamas, J. Nakayama and K. Sonomoto. 2021. Molecular characterization of the possible regulation of multiple bacteriocin production through a three-component regulatory system in Enterococcus faecium NKR-5-3. Journal of Bioscience and Bioengineering 131(2): 131-138.
Jørgensen, L.V. and H.H. Huss. 1998. Prevalence and growth of Listeria monocytogenes in naturally contaminated seafood. International Journal of Food Microbiology 42(1-2): 127-131.
Kamat, A.S. and P.M. Nair. 1996. Identification of Listeria innocua as a biological indicator for inactivation of Listeria monocytogenes by some meat processing treatments. Lebensmittel-Wissenschaft und-Technologie 29: 714-720.
Kathariou, S., R. Kanenaka, R.D. Allen, A.K. Fok and C. Mizumoto. 1995. Repression of motility and flagellin production at 37 °C is storage in Listeria monocytogenes than in the nonpathogenic species Listeria innocua. Canadian Journal of Microbiology 41: 572-575.
Khudhir, Z.S. 2019. The synergistic effect of pH and sodium citrate on the bacteriocidal activity of nisin against Staph aureus. International Journal of Veterinary Science 8(1): 49-53.
Kirtonia, K., M. Salauddin, K.K. Bharadwaj, S. Pati, A. Dey, M.A. Shariati and T. Sarkar. 2021. Bacteriocin: A new strategic antibiofilm agent in food industries. Biocatalysis and Agricultural Biotechnology 36: 102-141.
Kontominas, M.G., A.V. Badeka, I.S. Kosma and C.I. Nathanailides. 2021. Innovative seafood preservation technologies: Recent developments. Animals 11(1): 92. DOI: 10.3390/ani11010092.
Kumariya, R., A.K. Garsa, Y.S. Rajput, S.K. Sood, N. Akhtar and S. Patel. 2019. Bacteriocins: Classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microbiological Pathogenesis 128: 171-177.
Lambert, R.J.W., G.W. Hanlon and S.P. Denyer. 2004. The synergistic effect of EDTA/antimicrobial combinations on Pseudomonas aeruginosa. Journal of Applied Microbiology 96: 244-253.
Lappe, R., A.S. Motta, V. Sant’Anna and A. Brandelli. 2009. Inhibition of Salmonella Enteritidis by cerein 8A, EDTA and sodium lactate. International Journal of Food Microbiology 135: 312-316.
Long, C. and C.A. Phillips. 2003. The effect of sodium citrate, sodium lactate and nisin on the survival of Arcobacter butzleri NCTC 12481 on chicken. Food Microbiology 20: 495-502.
Lü, X., L. Yi, J. Dang, Y. Dang and B. Liu. 2014. Purification of novel bacteriocin produced by Lactobacillus coryniformis MXJ 32 for inhibiting bacterial foodborne pathogens including antibiotic-resistant microorganisms. Food Control 46: 264-271.
Maina, J.W., J.M. Mathara, G.M. Kikuvi and S.O. Ouma. 2017. Bacteriocins: Limiting factors to optimum activity. Journal of Food Security 5(2): 19-25.
Martin-Visscher, L.A., S. Yoganathan, C.S. Sit, C.T. Lohans and J.C. Vederas. 2011. The activity of bacteriocins from Carnobacterium maltaromaticum UAL307 against Gram-negative bacteria in combination with EDTA treatment. FEMS Microbiology Letters 317: 152-159.
Mayr-Harting, A., A.J. Hedges and R.C.W. Berkeley. 1972. Methods for studying bacteriocins, Vol. 7A. In: Methods in Microbiology (eds. T. Bergen and J.R. Norris), pp. 315-422. Academic Press, Inc., London, UK.
Mbandi, E. and L.A. Shelef. 2002. Enhanced antimicrobial effects of combination of lactate and diacetate on Listeria monocytogenes and Salmonella spp. in beef bologna. International Journal of Food Microbiology 76(3): 191-198.
Miettinen, M.K., A. Siitonen, P. Heiskanen, H. Haajanen, K.J. Björkroth and H.J. Korkeala. 1999. Molecular epidemiology of an outbreak of febrile gastroenteritis caused by Listeria monocytogenes in cold-smoked rainbow trout. Journal of Clinical Microbiology 37: 2358-2360.
Miller, A.J., J.E. Call and R.C. Whiting. 1993. Comparison of organic acid salt for Clostridium botulinum control in an uncured turkey product. Journal of Food Protection 56: 958-962.
Molinos, A.C., H. Abriouel, N. Ben Omar, E. Valdivia, R.L. López, M. Maqueda, M.M. Cañamero and A. Gálvez. 2005. Effect of immersion solutions containing enterocin AS-48 on Listeria monocytogenes in vegetable foods. Applied and Environmental Microbiology Journal 71(12): 7781-7787.
Molinos, A.C., H. Abriouel, R.L. López, N. Ben Omar, E. Valdivia and A. Gálvez. 2009. Enhanced bactericidal activity of enterocin AS-48 in combination with essential oils, natural bioactive compounds and chemical preservatives against Listeria monocytogenes in ready-to-eat salad. Food and Chemical Toxicology 47(9): 2216-2223.
Morey, A., J.W.J. Bowers, L.J. Bauermeister, M. Singh, T.S. Huang and S.R. McKee. 2014. Effect of salts of organic acids on Listeria monocytogenes, shelf life, meat quality, and consumer acceptability of beef frankfurters. Journal of Food Science 79(1): 54-60.
Muriana, P.M. 1996. Bacteriocins for control of Listeria spp. in food. Journal of Food Protection 59: 54-63.
Nes, I.F., D.A. Brede and D.B. Diep. 2013. Class II non-lantibiotic bacteriocins. In: Handbook of Biologically Active Peptides (ed. A.J. Kastin), pp. 85-92. Academic Press, Massachusetts, USA.
Ng, Z.J., M.A. Zarin, C.K. Lee and J.S. Tan. 2020. Application of bacteriocins in food preservation and infectious disease treatment for humans and livestock: A review. RSC Advances 10: 38937-38964.
Oladunjoye, A.O., O.A. Ijabadeniyi and S. Singh. 2016. Inactivation of Listeria monocytogenes ATCC 7644 on fresh-cut tomato using nisin in combinations with organic salts. Brazilian Journal Microbiology 47(3): 757-763.
O’ Sullivan, L., R.P. Ross and C. Hill. 2002. Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie 84: 593-604.
Qvist, S., K. Sehested and P. Zeuthen. 1994. Growth suppression of Listeria monocytogenes in a meat product. International Journal of Food Microbiology 24: 283-293.
Prudêncio, C.V., H.C. Mantovani and M.C.D. Vanetti. 2014. Inhibition of Salmonella Typhimurium by bovicin HC5 associated with chelating agents and surfactants. African Journal of Microbiology Research 8(1): 12-18.
Prudêncio, C.V., M.T. dos Santos and M.C.D. Vanetti. 2015. Strategies for the use of bacteriocins in Gram-negative bacteria: relevance in food microbiology. Journal of Food Science and Technology 52(9): 5408-5417.
Sangcharoen, N., W. Klaypradit and P. Wilaipun. 2017. Antimicrobial activity optimization of nisin, ascorbic acid and ethylenediamine tetraacetic acid disodium salt (EDTA) against Salmonella Enteritidis ATCC 13076 using response surface methodology. Agriculture and Natural Resources 51: 355-364.
Scannell, A.G.M., R.P. Ross, C. Hill and E.K. Arendt. 2000. An effective lacticin biopreservative in fresh pork sausage. Journal of Food Protection 63: 370-375.
Schillinger, U., R. Geisen and W.H. Holzapfel. 1996. Potential of antagonistic microorganisms for the biological preservation of foods. Trends in Food Science and Technology 7: 158-164.
Schjørring, S., L.S. Gillesberg, T. Jensen, A. Moura, J.S. Kjeldgaard, L. Müller, S. Thielke, A. Leclercq, M.M. Maury, M. Tourdjman, M.P. Donguy, M. Lecuit, S. Ethelberg and E.M. Nielsen. 2017. Cross-border outbreak of listeriosis caused by cold-smoked salmon, revealed by integrated surveillance and whole genome sequencing (WGS), Denmark and France, 2015 to 2017. Eurosurveillance 22: 1-5.
Seeliger, H.P.R. and D. Jones. 1986. Genus Listeria, regular, nonsporing Gram-positive rods. In: Bergey’s Manual of Systematic Bacteriology (eds. O. Kandler and N. Weiss), pp. 1235-1245. The Williams and Wilkins Co., Baltimore, USA.
Sidhu, P.K. and K. Nehra. 2019. Bacteriocin-nanoconjugates as emerging compounds for enhancing antimicrobial activity of bacteriocins. Journal of King Saud University-Science 31: 758-767.
Simons, A., K. Alhanout and R.E. Duval. 2020. Bacteriocins, antimicrobial peptides from bacterial origin: Overview of their biology and their impact against multidrug-resistant bacteria. Microorganisms 8: 639. DOI: 10.3390/microorganisms8050639.
Thai Food and Drug Administration. 2011. General Standard for Food Additives: GSFA 2011. http://newsser.fda.moph.go.th/food/file/BenefitAdmin/Book_ GSFA2011// Book_GSFA2011_9.pdf. Cited 1 Jul 2022.
Walkenhorst, W.F., J.N. Sundrud and J.M. Laviolette. 2014. Additivity and synergy between an antimicrobial peptide and inhibitory ions. Biochimica et Biophysica Acta 1838: 2234-2242.
Wang, Y., Y. Qin, Y. Zhang, R. Wu and P. Li. 2018. Antibacterial mechanism of plantaricin LPL-1, a novel class IIa bacteriocin against Listeria monocytogenes. Food Control 97: 87-93.
Wilaipun, P., T. Zendo, M. Sangjindavong, S. Nitisinprasert, V. Leelawatcharamas, J. Nakayama and K. Sonomoto. 2004. The two-synergistic peptide bacteriocin produced by Enterococcus faecium NKR 5-3 isolate from Thai fermented fish (Pla-ra). ScienceAsia 30: 115-122.
Wu, Y., X. Pang, Y. Wu, X. Liu and X. Zhang. 2022. Enterocins: Classification, synthesis, antibacterial mechanisms and food applications. Molecules 27(7): 2258. DOI: 10.3390/molecules27072258.
Zgheib, H., D. Drider and Y. Belguesmia. 2020. Broadening and enhancing bacteriocins activities by association with bioactive substances. International Journal of Environmental Research and Public Health 17(21): 7835. DOI: 10.3390/ijerph17217835.