Zeliha YILDIRIM, Yaselin İLK, Metin YILDIRIM, Kader TOKATLI, Nilgün ÖNCÜL

Inhibitory effect of enterocin KP in combination with sublethal factors on Escherichia coli O157:H7 or Salmonella Typhimurium in BHI broth and UHT milk

The effects of physical and chemical sublethal treatments on the antibacterial activity of enterocin KP produced by Enterococcus faecalis KP against Escherichia coli O157:H7 and Salmonella Typhimurium were investigated. Enterocin KP was not active against intact cells of E. coli O157:H7 or S. Typhimurium. However, the use of enterocin KP together with ethylenediaminetetraacetic acid (50 mM), sodium tripolyphosphate (50 mM), sublethal heating (60 °C for 10 min), cold shock (-20 °C for 2 h), or acid stress (mixture of 40% lactic acid, 16% propionic acid, 16% acetic acid) in BHI medium decreased the cell number of E. coli O157:H7 by 7.27, 6.28, 3.39, 3.06, 4.20 log and S. Typhimurium by 7.21, 6.20, 3.64, 3.38, 3.98 log cfu/mL, respectively. The combination of enterocin KP with ethylenediaminetetraacetic acid decreased the cell number of E. coli O157:H7 in UHT milk to undetectable level, enterocin KP plus sodium tripolyphosphate or enterocin KP plus sublethal heating caused a reduction by 6.07 and 5.68 log cycles. The results of this study showed that enterocin KP could be applied as a biopreservative to inhibit E. coli O157:H7 and S. Typhimurium in combination with physical and food grade chemical hurdles.

Anahtar Kelimeler:

Key words: Bacteriocin, enterocin KP, sublethal injury, gram-negative bacteria, UHT milk

Inhibitory effect of enterocin KP in combination with sublethal factors on Escherichia coli O157:H7 or Salmonella Typhimurium in BHI broth and UHT milk

Keywords:

Key words: Bacteriocin, enterocin KP, sublethal injury, gram-negative bacteria, UHT milk,

PDF

___

Abriouel H, Valdivia E, Gálvez A, Maqueda M (1998). Response of Salmonella choleraesuis LT2 spheroplasts and permeabilized cells to the bacteriocin AS-48. Appl Environ Microbiol 64: 4623–4626.
Alakomi H, Saarela M, Helander J (2003). Effect of EDTA on Salmonella enterica serovar Typhimurium involves a component not assignable to lipopolysaccharide release. Microbiol 149: 2015–2021.
Alakomi HL, Skytta E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM (2000). Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 66: 2001–2005.
Ananou S, Gálvez A, Martinez-Bueno M, Maqueda M, Valdivia E (2005). Synergistic effect of enterocin AS-48 in combination with outer membrane permeabilizing treatments against Escherichia coli O157:H7. J Appl Microbiol 99: 1364–1372.
Ananou S, Maqueda M, Martinez-Bueno M, Gálvez A, Valdivia E (2007). Bactericidal synergism through enterocin AS-48 and chemical preservatives against Staphylococcus aureus. Lett Appl Microbiol 45: 19–23.
Belfiore C, Castellano P, Vignolo G (2007). Reduction of Escherichia coli population following treatment with bacteriocins from lactic acid bacteria and chelators. Food Microbiol 24: 223–229.
Boziaris IS, Adams MR (1999). Effect of chelators and nisin produced in situ on inhibition and inactivation of Gram negatives. Int J Food Microbiol 53: 105–113.
Boziaris IS, Adams MR (2000). Transient sensitivity to nisin in coldshocked Gram negatives. Lett Appl Microbiol 31: 233–237.
Boziaris IS, Adams MR (2001). Temperature shock, injury and transient sensitivity to nisin in Gram negatives. J Appl Microbiol 91: 715–724.
Boziaris IS, Humpheson L, Adams MR (1998). Effect of nisin on heat injury and inactivation of Salmonella enteritidis PT4. Int J Food Microbiol 43: 7–13.
Bhunia A, Johnson MC, Ray B (1988). Purification, characterization and antimicrobial spectrum of a bacteriocin produced by Pediococcus acidilactici. J Appl Bacteriol 65: 261–268.
Cao-Hoang L, Dumont F, Marechal PA, Gervais P (2008). Rates of chilling to 0 degrees C: implications for the survival of microorganisms and relationship with membrane fluidity modifications. Appl Microbiol Biotechnol 77: 1379–1387.
Carneiro De Melo AMS, Cassar CL, Miles RJ (1998). Trisodium phosphate increases sensitivity of gram-negative bacteria to lysozyme and nisin. J Food Protect 61: 839–844.
Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001). Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71: 1–20.
Cutter CN, Siragusa GR (1995a). Population reductions of gram negative pathogens following treatments with nisin and chelators under various conditions. J Food Protect 58: 977–983.
Cutter CN, Siragusa GR (1995b). Treatments with nisin and chelators to reduce Salmonella and Escherichia coli on beef. J Food Protect 58: 1028–1030.
Drider D, Fimland G, Hechard Y, McMullen LM, Prévost H (2006). The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70: 564–582.
Fang TJ, Tsai HC (2003). Growth patterns of Escherichia coli O157:H7 in ground beef treated with nisin, chelators, organic acids and their combinations immobilized in calcium alginate gels. Food Microbiol 20: 243–253.
Gao Y, van Belkum MJ, Stiles ME (1999). The outer membrane of gram negative bacteria inhibits antibacterial activity of brochocin-C. Appl Environ Microbiol 65: 4329–4333.
Haest CWM, De Gier J, Van Es GA, Verkleij AJ, Van Deenen LM (1972). Fragility of the permeability barrier of Escherichia coli. Biochim Biophys Acta 288: 43–53.
Hancock R, Rozek A (2002). Role of membranes in the activities of antibacterial cationic peptides. FEMS Microbiol Lett 206: 143– 1
Helander IM, Mattila-Sandholm T (2000). Permeability barrier of the Gram-negative bacterial outer membrane with special reference to nisin. Int J Food Microbiol 60: 153–161.
Helander IM, von Wright A, Mattila-Sandholm TM (1997). Potential of lactic acid bacteria and novel antimicrobials against Gramnegative bacteria. Trends Food Sci Technol 8: 146–150.
Isleroglu H, Yildirim Z, Tokatli M, Nilgun O, Yildirim, M (2012). Partial characterisation of enterocin KP produced by Enterococcus faecalis KP, a cheese isolate. Int J Dairy Technol 65: 90–97.
Kalchayanand N, Sikes T, Dunne CP, Ray B (1994). Hydrostatic pressure and electroporation have increased bactericidal efficiency in combination with bacteriocins. Appl Environ Microbiol 60: 4174–4177.
Kalchayanand N, Hanlin MB, Ray B (1992). Sublethal injury makes gram-negative and resistant gram-positive bacteria sensitive to the bacteriocins, pediocin AcH and nisin. Lett Appl Microbiol 15: 239–243.
Lappe R, Motta AS, Sant’anna V, Brandelli A (2009). Inhibition of Salmonella Enteritidis by cerein 8A, EDTA and sodium lactate. Int J Food Microbiol 135: 312–316.
Leistner L (2000). Basic aspects of food preservation by hurdle technology. Int J Food Microbiol 55: 181–186.
Martin-Visscher LA, Yoganathan S, Sit CS, Lohans CT, Vederas JC (2011). The activity of bacteriocins from Carnobacterium maltaromaticum UAL307 against Gram-negative bacteria in combination with EDTA treatment. FEMS Microbial Lett 317: 152–159.
Moreno FMR, Leisner JJ, Tee LK, 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: 147–157. O smanağaoğlu Ö (2005). Sensitivity of sublethally injured gramnegative bacteria to pediocin P. J Food Safety 25: 266–275.
Przybylski KS, Witter LD (1979). Injury and recovery of Escherichia coli after sublethal acidification. Appl Environ Microbiol 37: 261–265.
Roth LA, Keenan D (1971). Acid injury in Escherichia coli. Can J Microbiol 17: 1005–1008.
Sampathkumar B, Khachatourians G, Korber D (2003). High pH during trisodium phosphate treatment causes membrane damage and destruction of Salmonella enterica serovar enteritidis. Appl Environ Microbiol 69: 122–129.
Schrödter K, Bettermann G, Staffel T, Wahl F, Klein T, Hofmann T (2008). Phosphoric acid and phosphates. Ullmann’s Enc Ind Chem, 26: 679–721.
Schved F, Henis Y, Juven BJ (1994). Response of spheroplasts and chelator-permeabilized cells of Gram-negative bacteria to the action of the bacteriocins pediocin SJ-1 and nisin. Int J Food Microbiol 21: 305–314.
Stevens KA, Sheldon BW, Klapes NA, Klaenhammer TR (1991). Nisin treatment for inactivation of Salmonella species and other gram-negative bacteria. Appl Environ Microbiol 57: 3613–3615.
Stiles ME (1996). Biopreservation by lactic acid bacteria. Antonie van Leeuw 70: 331–345.
Ter steeg PF, Hellemons JC, Kok AE (1999). Synergistic actions of nisin, sublethal ultrahigh pressure, and reduced temperature on bacteria and yeast. Appl Environ Microbiol 65: 4148–4154.
Vaara M (1992). Agents that increase the permeability of the outer membrane. Microbiol Rev 56: 395–411.
Yethon J, Whitfield C (2001). Lipopolysaccharide as a target for the development of novel therapeutics in Gram-negative bacteria. Curr Drug Targets Infect Disord 1: 91–106.