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Interactive effects of pH and temperature on the bacteriocin stability by response surface analysis

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Abstract

The combined influence of pH and temperature on bacteriocins produced by three lactic acid bacteria, Pediococcus pentosaceus MMZ26, Enterococcus faecium MMZ17 and Lactococcus lactis MMZ25, isolated from Tunisian traditional dry fermented meat was studied using a second order orthogonal factorial design and response-surface methodology (RSM). This method allows estimating the interactive effects of pH and temperature on the stability of each bacteriocin. The high heat stability of the three bacteriocins was demonstrated, with optimum values at light acidic pH around 5.0, temperature below 90°C and short incubation times. This study contributes to a better understanding of relation between bacteriocins production and stability in order to enhance their, in situ, application as a food and feed biopreservative in fermented and/or heated food products.

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References

  1. Caplice, E. and Fitzgerald, G.F., Food Fermentations: Role of Microorganisms in Food Production and Preservation, Int. J. Food Microbiol., 1999, vol. 50, pp. 31–149.

    Article  Google Scholar 

  2. Stiles, M.E., Biopreservation by Lactic Acid Bacteria, Antonie van Leeuwenhoek, 1996, vol. 70, pp. 331–345.

    Article  PubMed  CAS  Google Scholar 

  3. De Vuyst, L., Callewaert, R., and Crabbé, K., Primary Metabolite Kinetics of Bacteriocin Biosynthesis by Lactobacillus amylovorus and Evidence for Stimulation of Bacteriocin Production under Unfavourable Growth Conditions, Microbiology, 1996, vol. 142, pp. 817–827.

    Article  Google Scholar 

  4. Klaenhammer, T.R., Genetics of Bacteriocins Produced by Lactic Acid Bacteria, FEMS Microbiol Rev., 1993, vol. 12, pp. 39–86.

    PubMed  CAS  Google Scholar 

  5. De Kwaadsteniet, M., Todorov, S.D., Knoetze, H., and Dicks, L.M.T., Characterization of a 3944 Da Bacteriocin, Produced by Enterococcus mundtii ST15, with Activity Against Gram-Positive and Gram-Negative Bacteria, Int. J. Food Microbiol., 2005, vol. 105, pp. 433–444.

    Article  PubMed  Google Scholar 

  6. Cabo, M.L., Murado, M.A., Gonzalez, M.P., and Pastoriza, L., Effects of Aeration and pH Gradient on Nisin Production, a Mathematical Model, Enzyme Microb. Technol., 2001, vol. 29, pp. 264–273.

    Article  CAS  Google Scholar 

  7. Guerra, N.P., Agrasar, A.T., Macías, C.L., and Pastrana, L., Modelling the Fed-Batch Production of Pediocin Using Mussel Processing Wastes, Process Biochem., 2005, vol. 40, pp. 1071–1083.

    Article  CAS  Google Scholar 

  8. Dominguez, A.P.M., Bizani, D., Cladera-Olivera, F., and Brandelli, A., Cerein 8A Production in Soybean Protein Using Response Surface Methodology, Biochem. Eng. J., 2007, vol. 35, pp. 238–243.

    Article  CAS  Google Scholar 

  9. Myers, R.H. and Montgomery, D.C., Response Surface Methodology. Process and Products Optimization Using Designed Experiments, New York: Wiley, 2nd ed., 2002.

    Google Scholar 

  10. Pal, A. and Ramana, K.V., Isolation and Preliminary Characterization of a Non-Bacteriocin Antimicrobial Compound from Weissella paramesenteroides DFR-8 Isolated from Cucumber (Cucumis sativus), Process Biochem., 2009, vol. 44, pp. 499–503.

    Article  CAS  Google Scholar 

  11. Raza, W., Hongsheng, W., and Qirong, S., Use of Response Surface Methodology to Evaluate the Effect of Metal Ions (Ca2+, Ni2+, Mn2+, Cu2+) on Production of Antifungal Compounds by Paenibacillus polymyxa, Bioresour. Technol., 2010, vol. 101, pp. 1904–1912.

    Article  PubMed  CAS  Google Scholar 

  12. Qunhui, W., Hongzhi, M., Wenlong, X., Lijuan, G., Wenyu, Z., and Dexun, Z., Ethanol Production from Kitchen Garbage Using Response Surface Methodology, Biochem. Eng. J., 2008, vol. 39, pp. 604–610.

    Article  Google Scholar 

  13. Simonson, L., Salovaara, H., and Korhola, M., Response of Wheat Sourdough Parameters to Temperature, NaCl and Sucrose Variations, Food Microbiol., 2003, vol. 20, pp. 193–199.

    Article  CAS  Google Scholar 

  14. Xian-Yang, S., and Han-Qing, Y., Response Surface Analysis on the Effect of Cell Concentration and Light Intensity on Hydrogen Production by Rhodopseudomonas capsulate, Process Biochem., 2005, vol. 40, pp. 2475–2481.

    Article  Google Scholar 

  15. Delgado, A., Arroyo-Lo-pez, F.N., Brito, D., Peres, C, Fevereiro, P., and Garrido-Fernandez, A., Optimum Bacteriocin Production by Lactobacillus plantarum 17.2b Requires Absence of NaCl and Apparently Follows a Mixed Metabolite Kinetics, J. Biotechnol., 2007, vol. 130, pp. 193–201.

    Article  PubMed  CAS  Google Scholar 

  16. Cladera-O1ivera, F., Caron, G.R., and Brandelli, A., Bacteriocin Production by Bacillus licheniformis Strain P40 in Cheese Whey Using Response Surface Methodology, Biochem. Eng. J., 2004. vol. 21, pp. 53–58.

    Article  CAS  Google Scholar 

  17. Guerra, N.P. and Pastrana, L., Modelling the Influence of pH on the Kinetics of Both Nisin and Pediocin Production and Characterization of Their Functional Properties, Process Biochem., 2001, vol. 37, pp. 1005–1015.

    Article  Google Scholar 

  18. Ben Belgacem, Z., Dousset, X., Prévost, H., and Manai, M., Molecular Identification of the Microbiota of Traditional Tunisian Fermented Meat Based on the Heterogeneity and PCR-RFLP of the 16S–23S rRNA Gene Intergenic Spacer Region, Arch. Microbiol., 2009, vol. 191, pp. 711–720.

    Article  PubMed  CAS  Google Scholar 

  19. Cabo, M.L., Murado, M.A., González, M.P., and Pastoriza, L., A Method for Bacteriocin Quantification, J. Appl. Microbiol., 1999, vol. 87, pp. 907–914.

    Article  PubMed  CAS  Google Scholar 

  20. Akhnazarova, S. and Kafarov, V., Experiment Optimization in Chemistry and Chemical Engineering, Moscow: Mir, 1982.

    Google Scholar 

  21. Cheigh, C.I., Choi, H.J., Park, H., Kim, S.B., Kook, M.C., Kim, T.S., Hwang, J.K., and Pyun Y.T., Influence of Growth Conditions on the Production of a Nisin-Like Bacteriocin by Lactococcuslactis subsp. lactis A164 Isolated from Kimchi, J. Biotechnol., 2002, vol. 95, pp. 225–235.

    Article  PubMed  CAS  Google Scholar 

  22. Delgado, A., Brito, D., Peres, C., Arroyo-López, F.N., and Garrido-Fernández, A., Bacteriocin Production by Lactobacillus pentosus B96 can be Expressed as a Function of Temperature and NaCI Concentration, Food Microbiol., 2005, vol. 22, pp. 521–528.

    Article  CAS  Google Scholar 

  23. Drosinos, E.H., Mataragas, M., and Metaxopoulos, J., Modeling of Growth and Bacteriocin Production by Leuconostoc mesenteroides E131, Meat Science, 2006, vol. 74, pp. 690–696.

    Article  PubMed  CAS  Google Scholar 

  24. Mataragas, M., Metaxopoulos, J., Galiotou, M., and Drosinos, E.H., Influence of pH and Temperature on Growth and Bacteriocin Production by Leuconostoc mesenteroides L124 and Lactobacillus curvatus L442, Meat Science, 2003, vol. 64, pp. 265–271.

    Article  PubMed  CAS  Google Scholar 

  25. Van den Berghe, E., Skourtas, G., Tsakalidou, E., and De Vuyst, L., Streptococcus macedonicus ACA-DC 198 Produces the Lantibiotic, Macedocin at Temperature and pH Conditions that Prevail during Cheese Manufacture, Int. J. Food Microbiol., 2006, vol. 107, pp. 138–147.

    Article  PubMed  Google Scholar 

  26. Va-zquez, J.A., Jesu-s, M., Gonza-lez, M.P., and Murado, M.A., Bacteriocin Production and pH Gradient Some Mathematical Models and Their Problems, Enzyme Microb. Tech., 2005, vol. 37, pp. 54–67.

    Article  CAS  Google Scholar 

  27. Ryan, M.P., Rea, M.C., Hill, C., and Ross, P., An Application in Cheddar Cheese Manufactured for a Strain of Lactococcus lactis Producing a Novel Broad-Spectrum Bacteriocin, Lacticin 3147, Appl. Environ. Microbiol., 1996, vol. 62, pp. 612–619.

    PubMed  CAS  Google Scholar 

  28. Caldéron-Santoyo, M., Mendonza-García, P.G., García-Alvarado, M.A., and Escudero-Abarca, B.I., Effect of Physical Factors on the Production of Bacteriocin from Pediococcus acidilactici ITV26, J. Ind. Microbiol. Biotechnol., 2001, vol. 26, pp. 191–195.

    Article  PubMed  Google Scholar 

  29. Klostermaier, P., Scheyhing, C.H., Ehrmann, M., and Vogel, R.F., Mathematical Evaluation of Plantaricin Formation Supports an Auto-Induced Production Mechanism, Appl. Microbiol. Biotechnol., 1999, vol. 51, pp. 462–469.

    Article  CAS  Google Scholar 

  30. Krier, F., Revol-Junelles, A.M., and Germain, P., Influence of Temperature and pH on Production of Two Bacteriocins by Leuconostoc mesenteroides subsp. mesenteroides FR52 during Batch Fermentation, Appl. Microbiol. Biotechnol., 1998, vol. 50, pp. 359–363.

    Article  PubMed  CAS  Google Scholar 

  31. De Vuyst, L., and Vandamme, E.J., In: De Vuyst, L., and Vandamme, E.J. (Eds.), Bacteriocins of Lactic Acid Bacteria. Microbiology, Genetics and Applications. London, Blackie Academic and Professional, 1994, pp. 91–142.

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Correspondence to Z. Ben Belgacem.

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Ben Belgacem, Z., Rehaiem, A., Fajardo Bernárdez, P. et al. Interactive effects of pH and temperature on the bacteriocin stability by response surface analysis. Microbiology 81, 195–200 (2012). https://doi.org/10.1134/S002626171201002X

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