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Molecular Biotechnology

, Volume 60, Issue 9, pp 712–726 | Cite as

Lactic Acid Bacteria (LAB) and Their Bacteriocins as Alternative Biotechnological Tools to Control Listeria monocytogenes Biofilms in Food Processing Facilities

  • Anderson C. Camargo
  • Svetoslav D. Todorov
  • N. E. Chihib
  • D. Drider
  • Luís A. Nero
Review

Abstract

Bacteriocins are antimicrobial peptides produced by bacteria Gram-negative and Gram-positive, including lactic acid bacteria (LAB), organisms that are traditionally used in food preservation practices. Bacteriocins have been shown to have an aptitude as biofilm controlling agents in Listeria monocytogenes biofilms, a major risk for consumers and the food industry. Biofilms protect pathogens from sanitization procedures, allowing them to survive and persist in processing facilities, resulting in the cross-contamination of the end products. Studies have been undertaken on bacteriocinogenic LAB, their bacteriocins, and bioengineered bacteriocin derivatives for controlling L. monocytogenes biofilms on different surfaces through inhibition, competition, exclusion, and displacement. These alternative strategies can be considered promising in preventing the development of resistance to conventional sanitizers and disinfectants. Bacteriocins are “friendly” antimicrobial agents, and with high prevalence in nature, they do not have any known associated public health risk. Most trials have been carried out in vitro, on food contact materials such as polystyrene and stainless steel, while there have been few studies performed in situ to consolidate the results observed in vitro. There are strategies that can be employed for prevention and eradication of L. monocytogenes biofilms (such as the establishment of standard cleaning procedures using the available agents at proper concentrations). However, commercial cocktails using alternatives compounds recognized as safe and environmental friendly can be an alternative approach to be applied by the industries in the future.

Keywords

Bacteriocins Biofilm Lactic acid bacteria Listeria monocytogenes 

Notes

Acknowledgements

The authors thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). The authors would like also to mention the support of the Région des Hauts-de-France for the financial support through ALIBIOTECH grant.

References

  1. 1.
    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, 1–20.CrossRefPubMedGoogle Scholar
  2. 2.
    Cotter, P. D., Hill, C., & Ross, R. P. (2005). Bacteriocins: Developing innate immunity for food. Nature Reviews Microbiology, 3, 777.CrossRefPubMedGoogle Scholar
  3. 3.
    Line, J. E., Svetoch, E. A., Eruslanov, B. V., Perelygin, V. V., Mitsevich, E. V., Mitsevich, I. P., Levchuk, V. P., Svetoch, O. E., Seal, B. S., Siragusa, G. R., & Stern, N. J. (2008). Isolation and purification of enterocin E-760 with broad antimicrobial activity against Gram-positive and Gram-negative bacteria. Antimicrobial Agents and Chemotherapy, 52, 1094–1100.CrossRefPubMedGoogle Scholar
  4. 4.
    Nazef, L., Belguesmia, Y., Tani, A., Prévost, H., & Drider, D. (2008). Identification of lactic acid bacteria from poultry feces: Evidence on anti-Campylobacter and anti-Listeria activities. Poultry Science, 87, 329–334.CrossRefPubMedGoogle Scholar
  5. 5.
    Balciunas, E. M., Castillo Martinez, F. A., Todorov, S. D., Franco, B. D., Converti, A., Oliveira, R. P. (2013). Novel biotechnological applications of bacteriocins: A review. Food Control, 32, 134–142.CrossRefGoogle Scholar
  6. 6.
    Ibarreche, M., Castellano, P., Leclercq, A., & Vignolo, G. (2016). Control of Listeria monocytogenes biofilms on industrial surfaces by the bacteriocin-producing Lactobacillus sakei CRL1862. FEMS Microbiology Letters, 363, fnw118–fnw118.CrossRefGoogle Scholar
  7. 7.
    Chikindas, M. L., Weeks, R., Drider, D., Chistyakov, V. A., & Dicks, L. M. T. (2018). Functions and emerging applications of bacteriocins. Current Opinion in Biotechnology, 49, 23–28.CrossRefPubMedGoogle Scholar
  8. 8.
    Gou, J., Jung, L.-S., Lee, S.-H., & Ahn, J. (2011). Effects of nisin and acid on the inactivation and recovery of Listeria monocytogenes biofilms treated by high hydrostatic pressure. Food Science and Biotechnology, 20, 1361.CrossRefGoogle Scholar
  9. 9.
    Perez, R. H., Zendo, T., & Sonomoto, K. (2014). Novel bacteriocins from lactic acid bacteria (LAB): Various structures and applications. Microbial Cell Factories, 13, S3.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Smith, M. K., Draper, L. A., Hazelhoff, P.-J., Cotter, P. D., Ross, R. P., & Hill, C. (2016) A bioengineered nisin derivative, M21A, in combination with food grade additives eradicates biofilms of Listeria monocytogenes. Frontiers in Microbiology, 7, 1939.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Bolocan, A. S., Pennone, V., O’Connor, P. M., Coffey, A., Nicolau, A. I., McAuliffe, O., & Jordan, K. (2017). Inhibition of Listeria monocytogenes biofilms by bacteriocin-producing bacteria isolated from mushroom substrate. Journal of Applied Microbiology, 122, 279–293.CrossRefPubMedGoogle Scholar
  12. 12.
    Camargo, A. C., de Paula, O. A. L., Todorov, S. D., & Nero, L. A. (2016). In vitro evaluation of bacteriocins activity against Listeria monocytogenes biofilm formation. Applied Biochemistry and Biotechnology, 178, 1239–1251.CrossRefPubMedGoogle Scholar
  13. 13.
    Tan, X., Han, Y., Xiao, H., & Zhou, Z. (2017). Pediococcus Acidilactici inhibit biofilm formation of food-borne pathogens on abiotic surfaces. Transactions of Tianjin University, 23, 70–77.CrossRefGoogle Scholar
  14. 14.
    Khelissa, S., Abdallah, M., Jama, C., Faille, C., & Chihib, N.-E. (2017). Bacterial contamination and biofilm formation on abiotic surfaces and strategies to overcome their persistence. Journal of Materials and Environmental Science, 8, 3326–3346.Google Scholar
  15. 15.
    Abdallah, M., Benoliel, C., Drider, D., Dhulster, P., & Chihib, N.-E. (2014). Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Archives of Microbiology, 196, 453–472.CrossRefPubMedGoogle Scholar
  16. 16.
    Ferreira, V., Wiedmann, M., Teixeira, P., & Stasiewicz, M. J. (2014). Listeria monocytogenes persistence in food-associated environments: Epidemiology, strain characteristics, and implications for public health. Journal of Food Protection, 77, 150–170.CrossRefPubMedGoogle Scholar
  17. 17.
    To, M. S., Favrin, S., Romanova, N., & Griffiths, M. W. (2002). Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Applied and Environmental Microbiology, 68, 5258–5264.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Yang, H., Kendall, P. A., Medeiros, L. C., & Sofos, J. N. (2009). Efficacy of sanitizing agents against Listeria monocytogenes biofilms on high-density polyethylene cutting board surfaces. Journal of Food Protection, 72, 990–998.CrossRefPubMedGoogle Scholar
  19. 19.
    Møretrø, T., & Langsrud, S. (2004). Listeria monocytogenes: Biofilm formation and persistence in food-processing environments. Biofilms, 1, 107–121.CrossRefGoogle Scholar
  20. 20.
    Simões, M., Simões, L. C., & Vieira, M. J. (2010). A review of current and emergent biofilm control strategies. LWT Food Science and Technology, 43, 573–583.CrossRefGoogle Scholar
  21. 21.
    Camargo, A. C., Woodward, J. J., Call, D. R., & Nero, L. A. (2017). Listeria monocytogenes in food-processing facilities, food contamination, and human listeriosis: The brazilian scenario. Foodborne Pathogens and Disease, 14, 623–636.CrossRefPubMedGoogle Scholar
  22. 22.
    Drider, D., Bendali, F., Naghmouchi, K., & Chikindas, M. L. (2016). Bacteriocins: Not only antibacterial agents. Probiotics and Antimicrobial Proteins, 8, 177–182.CrossRefPubMedGoogle Scholar
  23. 23.
    Egan, K., Field, D., Rea, M. C., Ross, R. P., Hill, C., & Cotter, P. D. (2016). Bacteriocins: Novel solutions to age old spore-related problems? Frontiers in Microbiology, 7, 461.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Alvarez-Sieiro, P., Montalbán-López, M., Mu, D., & Kuipers, O. P. (2016). Bacteriocins of lactic acid bacteria: Extending the family. Applied Microbiology and Biotechnology, 100, 2939–2951.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Yang, S.-C., Lin, C.-H., Sung, C. T., & Fang, J.-Y. (2014). Antibacterial activities of bacteriocins: Application in foods and pharmaceuticals. Frontiers in Microbiology, 5, 241.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Favaro, L., Barretto Penna, A. L., Todorov, S. D. (2015). Bacteriocinogenic LAB from cheeses—application in biopreservation? Trends in Food Science & Technology, 41, 37–48.CrossRefGoogle Scholar
  27. 27.
    Heng, N. C. K., Wescombe, P. A., Burton, J. P., Jack, R. W., & Tagg, J. R. (2007). The diversity of bacteriocins in Gram-positive bacteria. In M. A. Riley & M. A. Chavan (Eds.), Bacteriocins: Ecology and evolution (pp. 45–92). Berlin: Springer.CrossRefGoogle Scholar
  28. 28.
    Brötz, H., Josten, M., Wiedemann, I., Schneider, U., Götz, F., Bierbaum, G., & Sahl, H.-G. (1998). Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics. Molecular Microbiology, 30, 317–327.CrossRefPubMedGoogle Scholar
  29. 29.
    Breukink, E., Wiedemann, I., Kraaij, C. v., Kuipers, O. P., Sahl, H.-G., & de Kruijff, B. (1999). Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science, 286, 2361–2364.CrossRefPubMedGoogle Scholar
  30. 30.
    Healy, B., Field, D., O’Connor, P. M., Hill, C., Cotter, P. D., & Ross, R. P. (2013) Intensive mutagenesis of the nisin hinge leads to the rational design of enhanced derivatives. PLoS ONE 8, e79563.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Wiedemann, I., Breukink, E., van Kraaij, C., Kuipers, O. P., Bierbaum, G., de Kruijff, B., & Sahl, H.-G. (2001). Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. Journal of Biological Chemistry, 276, 1772–1779.CrossRefPubMedGoogle Scholar
  32. 32.
    Hsu, S.-T. D., Breukink, E., Tischenko, E., Lutters, M. A. G., de Kruijff, B., Kaptein, R., Bonvin, A. M. J. J., & van Nuland, N. A. J. (2004). The nisin–lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nature Structural & Molecular Biology, 11, 963.CrossRefGoogle Scholar
  33. 33.
    Yuan, J., Zhang, Z.-Z., Chen, X.-Z., Yang, W., & Huan, L.-D. (2004). Site-directed mutagenesis of the hinge region of nisinZ and properties of nisinZ mutants. Applied Microbiology and Biotechnology, 64, 806–815.CrossRefPubMedGoogle Scholar
  34. 34.
    Dischinger, J., Basi Chipalu, S., Bierbaum, G. (2014). Lantibiotics: Promising candidates for future applications in health care. International Journal of Medical Microbiology, 304, 51–62.CrossRefPubMedGoogle Scholar
  35. 35.
    Chatterjee, C., Paul, M., Xie, L., & van der Donk, W. A. (2005). Biosynthesis and mode of action of lantibiotics. Chemical Reviews, 105, 633–684.CrossRefPubMedGoogle Scholar
  36. 36.
    Alkhatib, Z., Abts, A., Mavaro, A., Schmitt, L., & Smits, S. H. J. (2012). Lantibiotics: How do producers become self-protected? Journal of Biotechnology, 159, 145–154.CrossRefPubMedGoogle Scholar
  37. 37.
    Robichon, D., Gouin, E., Débarbouillé, M., Cossart, P., Cenatiempo, Y., & Héchard, Y. (1997). The rpoN (sigma54) gene from Listeria monocytogenes is involved in resistance to mesentericin Y105, an antibacterial peptide from Leuconostoc mesenteroides. Journal of Bacteriology, 179, 7591–7594.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Gravesen, A., Ramnath, M., Rechinger, K. B., Andersen, N., Jänsch, L., Héchard, Y., Hastings, J. W., & Knøchel, S. (2002). High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiology, 148, 2361–2369.CrossRefPubMedGoogle Scholar
  39. 39.
    Drider, D., Fimland, G., Héchard, Y., McMullen, L. M., & Prévost, H. (2006). The continuing story of class IIa bacteriocins. Microbiology and Molecular Biology Reviews, 70, 564–582.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Cui, Y., Zhang, C., Wang, Y., Shi, J., Zhang, L., Ding, Z., Qu, X., & Cui, H. (2012). Class IIa bacteriocins: Diversity and new developments. International Journal of Molecular Sciences, 13, 16668.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Todorov, S. D. (2009). Bacteriocins from Lactobacillus plantarum production, genetic organization and mode of action. Brazilian Journal of Microbiology, 40, 209–221.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Mokoena, M. P. (2017). Lactic acid bacteria and their bacteriocins: Classification, biosynthesis and applications against uropathogens: A mini-review. Molecules, 22, 1255.CrossRefGoogle Scholar
  43. 43.
    Nilsen, T., Nes, I. F., & Holo, H. (2003). Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Applied and Environmental Microbiology, 69, 2975–2984.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Joerger, M. C., & Klaenhammer, T. R. (1990). Cloning, expression, and nucleotide sequence of the Lactobacillus helveticus 481 gene encoding the bacteriocin helveticin J. Journal of Bacteriology, 172, 6339–6347.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Belguesmia, Y., Madi, A., Sperandio, D., Merieau, A., Feuilloley, M., Prévost, H., Drider, D., & Connil, N. (2011). Growing insights into the safety of bacteriocins: The case of enterocin S37. Research in Microbiology, 162, 159–163.CrossRefPubMedGoogle Scholar
  46. 46.
    Gálvez, A., Abriouel, H., López, R. L., & Omar, N. B. (2007). Bacteriocin-based strategies for food biopreservation. International Journal of Food Microbiology, 120, 51–70.CrossRefPubMedGoogle Scholar
  47. 47.
    Settanni, L., & Corsetti, A. (2008). Application of bacteriocins in vegetable food biopreservation. International Journal of Food Microbiology, 121, 123–138.CrossRefPubMedGoogle Scholar
  48. 48.
    Suda, S., Cotter, P.D., Hill, C., Paul Ross, R. (2012). Lacticin 3147—biosynthesis, molecular analysis, immunity, bioengineering and applications. Current Protein and Peptide Science, 13, 193–204.CrossRefPubMedGoogle Scholar
  49. 49.
    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, 68, 2845–2857.CrossRefPubMedGoogle Scholar
  50. 50.
    Chmielewski, R. A. N., & Frank, J. F. (2003). Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2, 22–32.CrossRefGoogle Scholar
  51. 51.
    Jefferson, K. K. (2004). What drives bacteria to produce a biofilm? FEMS Microbiology Letters, 236, 163–173.CrossRefPubMedGoogle Scholar
  52. 52.
    Giaouris, E., Heir, E., Hébraud, M., Chorianopoulos, N., Langsrud, S., Møretrø, T., Habimana, O., Desvaux, M., Renier, S., & Nychas, G.-J. (2014). Attachment and biofilm formation by foodborne bacteria in meat processing environments: Causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Science, 97, 298–309.CrossRefPubMedGoogle Scholar
  53. 53.
    Srey, S., Jahid, I. K., & Ha, S.-D. (2013). Biofilm formation in food industries: A food safety concern. Food Control, 31, 572–585.CrossRefGoogle Scholar
  54. 54.
    Norwood, D. E., & Gilmour, A. (1999). Adherence of Listeria monocytogenes strains to stainless steel coupons. Journal of Applied Microbiology, 86, 576–582.CrossRefPubMedGoogle Scholar
  55. 55.
    Frank, J. F., & Koffi, R. A. (1990). Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to surfactant sanitizers and heat. Journal of Food Protection, 53, 550–554.CrossRefGoogle Scholar
  56. 56.
    Lee, S., & Frank, J. F. (1991). Inactivation of surface-adherent Listeria monocytogenes hypochlorite and heat. Journal of Food Protection, 54, 4–6.CrossRefGoogle Scholar
  57. 57.
    Camargo, A. C., Dias, M. R., Cossi, M. V., Lanna, F. G., Cavicchioli, V. Q., Vallim, D. C., Pinto, P. S., Hofer, E., & Nero, L. A. (2015). Serotypes and pulsotypes diversity of Listeria monocytogenes in a beef-processing environment. Foodborne Pathogens and Disease, 12, 323–326.CrossRefPubMedGoogle Scholar
  58. 58.
    Leong, D., Alvarez-Ordóñez, A., & Jordan, K. (2014). Monitoring occurrence and persistence of Listeria monocytogenes in foods and food processing environments in the Republic of Ireland. Frontiers in Microbiology, 5, 436.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Gandhi, M., & Chikindas, M. L. (2007). Listeria: A foodborne pathogen that knows how to survive. International Journal of Food Microbiology, 113, 1–15.CrossRefPubMedGoogle Scholar
  60. 60.
    Vatanyoopaisarn, S., Nazli, A., Dodd, C. E. R., Rees, C. E. D., & Waites, W. M. (2000). Effect of flagella on initial attachment of Listeria monocytogenes to stainless steel. Applied and Environmental Microbiology, 66, 860–863.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Lemon, K. P., Higgins, D. E., & Kolter, R. (2007). Flagellar motility is critical for Listeria monocytogenes biofilm formation. Journal of Bacteriology, 189, 4418–4424.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lemon, K. P., Freitag, N. E., & Kolter, R. (2010). The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. Journal of Bacteriology, 192, 3969–3976.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Luo, Q., Shang, J., Feng, X., Guo, X., Zhang, L., & Zhou, Q. (2013). PrfA led to reduced biofilm formation and contributed to altered gene expression patterns in biofilm-forming Listeria monocytogenes. Current Microbiology, 67, 372–378.CrossRefPubMedGoogle Scholar
  64. 64.
    Belval, S. C., Gal, L., Margiewes, S., Garmyn, D., Piveteau, P., & Guzzo, J. (2006). Assessment of the roles of LuxS, S-ribosyl homocysteine, and autoinducer 2 in cell attachment during biofilm formation by Listeria monocytogenes EGD-e. Applied and Environmental Microbiology, 72, 2644–2650.CrossRefGoogle Scholar
  65. 65.
    Rieu, A., Weidmann, S., Garmyn, D., Piveteau, P., & Guzzo, J. (2007). Agr system of Listeria monocytogenes EGD-e: Role in adherence and differential expression pattern. Applied and Environmental Microbiology, 73, 6125–6133.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Taylor, C. M., Beresford, M., Epton, H. A. S., Sigee, D. C., Shama, G., Andrew, P. W., & Roberts, I. S. (2002). Listeria monocytogenesrelA and hpt mutants are impaired in surface-attached growth and virulence. Journal of Bacteriology, 184, 621–628.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Renier, S., Chagnot, C., Deschamps, J., Caccia, N., Szlavik, J., Joyce, S. A., Popowska, M., Hill, C., Knøchel, S., Briandet, R., Hébraud, M., & Desvaux, M. (2014). Inactivation of the SecA2 protein export pathway in Listeria monocytogenes promotes cell aggregation, impacts biofilm architecture and induces biofilm formation in environmental condition. Environmental Microbiology, 16, 1176–1192.CrossRefPubMedGoogle Scholar
  68. 68.
    Jordan, S. J., Perni, S., Glenn, S., Fernandes, I., Barbosa, M., Sol, M., Tenreiro, R. P., Chambel, L., Barata, B., Zilhao, I., Aldsworth, T. G., Adriao, A., Faleiro, M. L., Shama, G., & Andrew, P. W. (2008). Listeria monocytogenes biofilm-associated protein (BapL) may contribute to surface attachment of L. monocytogenes but is absent from many field isolates. Applied and Environmental Microbiology, 74, 5451–5456.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Zhu, X., Long, F., Chen, Y., Knøchel, S., She, Q., & Shi, X. (2008). A putative ABC transporter is involved in negative regulation of biofilm formation by Listeria monocytogenes. Applied and Environmental Microbiology, 74, 7675–7683.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Harmsen, M., Lappann, M., Knøchel, S., & Molin, S. (2010). Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Applied and Environmental Microbiology, 76, 2271–2279.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Kocot, A. M., & Olszewska, M. A. (2017). Biofilm formation and microscopic analysis of biofilms formed by Listeria monocytogenes in a food processing context. LWT Food Science and Technology, 84, 47–57.CrossRefGoogle Scholar
  72. 72.
    Chmielewski, R. A. N., & Frank, J. F. (2007) Inactivation of Listeria monocytogenes biofilms using chemical sanitizers and heat. In Blaschek, H.P., Wang, H.H., Agle, M.E. (Eds) Biofilms in the food environment (pp. 73–104). Ames: Blackwell Publishing.Google Scholar
  73. 73.
    Robbins, J. b., Fisher, C. w., Moltz, A. g., & Martin, S. e. (2005). Elimination of Listeria monocytogenes biofilms by ozone, chlorine, and hydrogen peroxide. Journal of Food Protection, 68, 494–498.CrossRefPubMedGoogle Scholar
  74. 74.
    Chavant, P., Gaillard-Martinie, B., & Hébraud, M. (2004). Antimicrobial effects of sanitizers against planktonic and sessile Listeria monocytogenes cells according to the growth phase. FEMS Microbiology Letters, 236, 241–248.CrossRefPubMedGoogle Scholar
  75. 75.
    Olszewska, M. A., Zhao, T., & Doyle, M. P. (2016). Inactivation and induction of sublethal injury of Listeria monocytogenes in biofilm treated with various sanitizers. Food Control, 70, 371–379.CrossRefGoogle Scholar
  76. 76.
    Poimenidou, S. V., Chrysadakou, M., Tzakoniati, A., Bikouli, V. C., Nychas, G.-J., & Skandamis, P. N. (2016). Variability of Listeria monocytogenes strains in biofilm formation on stainless steel and polystyrene materials and resistance to peracetic acid and quaternary ammonium compounds. International Journal of Food Microbiology, 237, 164–171.CrossRefPubMedGoogle Scholar
  77. 77.
    Rodríguez-López, P., & Cabo, M. L. (2017). Tolerance development in Listeria monocytogenes-Escherichia coli dual-species biofilms after sublethal exposures to pronase-benzalkonium chloride combined treatments. Food Microbiology, 67, 58–66.CrossRefPubMedGoogle Scholar
  78. 78.
    Pan, Y., Breidt, F., & Kathariou, S. (2006). Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Applied and Environmental Microbiology, 72, 7711–7717.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Kovacevic, J., Ziegler, J., Wałecka-Zacharska, E., Reimer, A., Kitts, D. D., & Gilmour, M. W. (2016). Tolerance of Listeria monocytogenes to quaternary ammonium sanitizers is mediated by a novel efflux pump encoded by emrE. Applied and Environmental Microbiology, 82, 939–953.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Jiang, X., Yu, T., Liang, Y., Ji, S., Guo, X., Ma, J., & Zhou, L. (2016). Efflux pump-mediated benzalkonium chloride resistance in Listeria monocytogenes isolated from retail food. International Journal of Food Microbiology, 217, 141–145.CrossRefPubMedGoogle Scholar
  81. 81.
    Ait Ouali, F., Al Kassaa, I., Cudennec, B., Abdallah, M., Bendali, F., Sadoun, D., Chihib, N.E., Drider, D. (2014). Identification of lactobacilli with inhibitory effect on biofilm formation by pathogenic bacteria on stainless steel surfaces. International Journal of Food Microbiology, 191, 116–124.CrossRefPubMedGoogle Scholar
  82. 82.
    García-Almendárez, B. E., Cann, I. K. O., Martin, S. E., Guerrero-Legarreta, I., & Regalado, C. (2008). Effect of Lactococcus lactis UQ2 and its bacteriocin on Listeria monocytogenes biofilms. Food Control, 19, 670–680.CrossRefGoogle Scholar
  83. 83.
    Leriche, V., Chassaing, D., & Carpentier, B. (1999). Behaviour of L. monocytogenes in an artificially made biofilm of a nisin-producing strain of Lactococcus lactis. International Journal of Food Microbiology, 51, 169–182.CrossRefPubMedGoogle Scholar
  84. 84.
    Al-Seraih, A., Belguesmia, Y., Baah, J., Szunerits, S., Boukherroub, R., & Drider, D. (2017). Enterocin B3A-B3B produced by LAB collected from infant faeces: Potential utilization in the food industry for Listeria monocytogenes biofilm management. Antonie van Leeuwenhoek, 110, 205–219.CrossRefPubMedGoogle Scholar
  85. 85.
    Guerrieri, E., de Niederhäusern, S., Messi, P., Sabia, C., Iseppi, R., Anacarso, I., & Bondi, M. (2009). Use of lactic acid bacteria (LAB) biofilms for the control of Listeria monocytogenes in a small-scale model. Food Control, 20, 861–865.CrossRefGoogle Scholar
  86. 86.
    Ibarreche, M., Castellano, P., & Vignolo, G. (2014). Evaluation of anti-Listeria meat borne Lactobacillus for biofilm formation on selected abiotic surfaces. Meat Science, 96, 295–303.CrossRefGoogle Scholar
  87. 87.
    Winkelströter, L. K., Gomes, B. C., Thomaz, M. R. S., Souza, V. M., & De Martinis, E. C. P. (2011). Lactobacillus sakei 1 and its bacteriocin influence adhesion of Listeria monocytogenes on stainless steel surface. Food Control, 22, 1404–1407.CrossRefGoogle Scholar
  88. 88.
    O’Connor, P. M., O’Shea, E. F., Guinane, C. M., O’Sullivan, O., Cotter, P. D., Ross, R. P., & Hill, C. (2015). Nisin H is a new nisin variant produced by the gut-derived strain Streptococcus hyointestinalis DPC6484. Applied and Environmental Microbiology, 81, 3953–3960.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Gharsallaoui, A., Oulahal, N., Joly, C., & Degraeve, P. (2016). Nisin as a food preservative: part 1: Physicochemical properties, antimicrobial activity, and main uses. Critical Reviews in Food Science and Nutrition, 56, 1262–1274.CrossRefPubMedGoogle Scholar
  90. 90.
    Deegan, L. H., Cotter, P. D., Hill, C., & Ross, P. (2006). Bacteriocins: Biological tools for bio-preservation and shelf-life extension. International Dairy Journal, 16, 1058–1071.CrossRefGoogle Scholar
  91. 91.
    Karam, L., Jama, C., Mamede, A.-S., Boukla, S., Dhulster, P., & Chihib, N.-E. (2013). Nisin-activated hydrophobic and hydrophilic surfaces: Assessment of peptide adsorption and antibacterial activity against some food pathogens. Applied Microbiology and Biotechnology, 97, 10321–10328.CrossRefPubMedGoogle Scholar
  92. 92.
    Mulders, J. W. M., Boerrigter, I. J., Rollema, H. S., Siezen, R. J., & de Vos, W. M. (1991). Identification and characterization of the lantibiotic nisin Z, a natural nisin variant. European Journal of Biochemistry, 201, 581–584.CrossRefPubMedGoogle Scholar
  93. 93.
    Minei, C. C., Gomes, B. C., Ratti, R. P., D’angelis, C. E. M., & De Martinis, E. C. P. (2008). Influence of peroxyacetic acid and nisin and coculture with Enterococcus faecium on Listeria monocytogenes biofilm formation. Journal of Food Protection, 71, 634–638.CrossRefPubMedGoogle Scholar
  94. 94.
    Okuda, K., Zendo, T., Sugimoto, S., Iwase, T., Tajima, A., Yamada, S., Sonomoto, K., & Mizunoe, Y. (2013). Effects of bacteriocins on methicillin-resistant Staphylococcus aureus Biofilm. Antimicrobial Agents and Chemotherapy, 57, 5572–5579.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Mahdavi, M., Jalali, M., & Kermanshahi, R. K. (2009). The effect of nisin on biofilm forming foodborne bacteria using microtiter plate method. Research in Pharmaceutical Sciences, 6, 113–118.Google Scholar
  96. 96.
    Pimentel-Filho, N. d. J., Martins, M. C., d., F., Nogueira, G. B., Mantovani, H. C., & Vanetti, M. C. D. (2014). Bovicin HC5 and nisin reduce Staphylococcus aureus adhesion to polystyrene and change the hydrophobicity profile and Gibbs free energy of adhesion. International Journal of Food Microbiology, 190, 1–8.CrossRefGoogle Scholar
  97. 97.
    Mazzotta, A. S., & Montville, T. J. (1997). Nisin induces changes in membrane fatty acid composition of Listeria monocytogenes nisin-resistant strains at 10 °C and 30 °C. Journal of Applied Microbiology, 82, 32–38.CrossRefPubMedGoogle Scholar
  98. 98.
    Naghmouchi, K., Belguesmia, Y., Baah, J., Teather, R., & Drider, D. (2011). Antibacterial activity of class I and IIa bacteriocins combined with polymyxin E against resistant variants of Listeria monocytogenes and Escherichia coli. Research in Microbiology, 162, 99–107.CrossRefPubMedGoogle Scholar
  99. 99.
    Fontana, C., Cocconcelli, P. S., Vignolo, G., & Saavedra, L. (2015). Occurrence of antilisterial structural bacteriocins genes in meat borne lactic acid bacteria. Food Control, 47, 53–59.CrossRefGoogle Scholar
  100. 100.
    Messi, P., Bondi, M., Sabia, C., Battini, R., & Manicardi, G. (2001). Detection and preliminary characterization of a bacteriocin (plantaricin 35d) produced by a Lactobacillus plantarum strain. International Journal of Food Microbiology, 64, 193–198.CrossRefPubMedGoogle Scholar
  101. 101.
    Ben Slama, R., Kouidhi, B., Zmantar, T., Chaieb, K., & Bakhrouf, A. (2013). Anti-listerial and anti-biofilm activities of potential probiotic Lactobacillus strains isolated from Tunisian traditional fermented food. Journal of Food Safety, 33, 8–16.CrossRefGoogle Scholar
  102. 102.
    Tomé, E., Todorov, S. D., Gibbs, P. A., & Teixeira, P. C. (2009). Partial characterization of nine bacteriocins produced by lactic acid bacteria isolated from cold-smoked salmon with activity against Listeria monocytogenes. Food Biotechnology, 23, 50–73.CrossRefGoogle Scholar
  103. 103.
    Todorov, S. D., de Paula, O. A. L., Camargo, A. C., Lopes, D. A., & Nero, L. A. (2017). Combined effect of bacteriocin produced by Lactobacillus plantarum ST8SH and vancomycin, propolis or EDTA for controlling biofilm development by Listeria monocytogenes. Revista Argentina de Microbiología.  https://doi.org/10.1016/j.ram.2017.04.011 CrossRefPubMedGoogle Scholar
  104. 104.
    Winkelströter, L. K., Tulini, F. L., & De Martinis, E. C. P. (2015). Identification of the bacteriocin produced by cheese isolate Lactobacillus paraplantarum FT259 and its potential influence on Listeria monocytogenes biofilm formation. LWT Food Science and Technology, 64, 586–592.CrossRefGoogle Scholar
  105. 105.
    Yi, L., Luo, L., & Lü, X. (2018). Heterologous expression of two novel bacteriocins produced by Lactobacillus crustorum MN047 and application of BM1157 in control of Listeria monocytogenes. Food Control, 86, 374–382.CrossRefGoogle Scholar
  106. 106.
    Cintas, L. M., Casaus, P., Fernández, M. F., & Hernández, P. E. (1998). Comparative antimicrobial activity of enterocin L50, pediocin PA-1, nisin A and lactocin S against spoilage and foodborne pathogenic bacteria. Food Microbiology, 15, 289–298.CrossRefGoogle Scholar
  107. 107.
    Rodríguez, J. M., Martínez, M. I., & Kok, J. (2002). Pediocin PA-1, a wide-spectrum bacteriocin from lactic acid bacteria. Critical Reviews in Food Science and Nutrition, 42, 91–121.CrossRefPubMedGoogle Scholar
  108. 108.
    Blay, G. L., Lacroix, C., Zihler, A., & Fliss, I. (2007). In vitro inhibition activity of nisin A, nisin Z, pediocin PA-1 and antibiotics against common intestinal bacteria. Letters in Applied Microbiology, 45, 252–257.CrossRefPubMedGoogle Scholar
  109. 109.
    Santiago-Silva, P., Soares, N. F. F., Nóbrega, J. E., Júnior, M. A. W., Barbosa, K. B. F., Volp, A. C. P., Zerdas, E. R. M. A., & Würlitzer, N. J. (2009). Antimicrobial efficiency of film incorporated with pediocin (ALTA® 2351) on preservation of sliced ham. Food Control, 20, 85–89.CrossRefGoogle Scholar
  110. 110.
    Woraprayote, W., Kingcha, Y., Amonphanpokin, P., Kruenate, J., Zendo, T., Sonomoto, K., Benjakul, S., & Visessanguan, W. (2013). Anti-listeria activity of poly(lactic acid)/sawdust particle biocomposite film impregnated with pediocin PA-1/AcH and its use in raw sliced pork. International Journal of Food Microbiology, 167, 229–235.CrossRefPubMedGoogle Scholar
  111. 111.
    Espitia, P. J. P., Otoni, C. G., & Soares, N. F. F. (2016). Chapter 36—Pediocin applications in antimicrobial food packaging systems in Antimicrobial Food Packaging (pp. 445–454). San Diego: Academic Press.Google Scholar
  112. 112.
    Verma, S. K., Sood, S. K., Saini, R. K., & Saini, N. (2017). Pediocin PA-1 containing fermented cheese whey reduces total viable count of raw buffalo (Bubalis bubalus) milk. LWT Food Science and Technology, 83, 193–200.CrossRefGoogle Scholar
  113. 113.
    Giraffa, G. (1995). Enterococcal bacteriocins: Their potential as anti-Listeria factors in dairy technology. Food Microbiology, 12, 291–299.CrossRefGoogle Scholar
  114. 114.
    Arihara, K., Cassens, R. G., & Luchansky, J. B. (1993). Characterization of bacteriocins from Enterococcus faecium with activity against Listeria monocytogenes. International Journal of Food Microbiology, 19, 123–134.CrossRefPubMedGoogle Scholar
  115. 115.
    Khan, H., Flint, S., & Yu, P.-L. (2010). Enterocins in food preservation. International Journal of Food Microbiology, 141, 1–10.CrossRefPubMedGoogle Scholar
  116. 116.
    Abriouel, H., Lucas, R., Omar, N. B., Valdivia, E., & Gálvez, A. (2010). Potential applications of the cyclic peptide enterocin AS-48 in the preservation of vegetable foods and beverages. Probiotics and Antimicrobial Proteins, 2, 77–89.CrossRefPubMedGoogle Scholar
  117. 117.
    Ananou, S., Garriga, M., Jofré, A., Aymerich, T., Gálvez, A., Maqueda, M., Martínez-Bueno, M., & Valdivia, E. (2010). Combined effect of enterocin AS-48 and high hydrostatic pressure to control food-borne pathogens inoculated in low acid fermented sausages. Meat Science, 84, 594–600.CrossRefPubMedGoogle Scholar
  118. 118.
    Caballero Gómez, N., Abriouel, H., Grande, M. J., Pérez Pulido, R., & Gálvez, A. (2012). Effect of enterocin AS-48 in combination with biocides on planktonic and sessile Listeria monocytogenes. Food Microbiology, 30, 51–58.CrossRefGoogle Scholar
  119. 119.
    Field, D., Begley, M., O’Connor, P. M., Daly, K. M., Hugenholtz, F., Cotter, P. D., Hill, C., & Ross, R. P. (2012). Bioengineered nisin A derivatives with enhanced activity against both Gram positive and Gram negative pathogens. PLoS ONE, 7, e46884.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Field, D., Cotter, P. D., Hill, C., & Ross, R. P. (2015) Bioengineering lantibiotics for therapeutic success. Frontiers in Microbiology, 6, 1363.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Field, D., Hill, C., Cotter, P. D., & Ross, R. P. (2010). The dawning of a ‘Golden era’ in lantibiotic bioengineering. Molecular Microbiology, 78, 1077–1087.CrossRefPubMedGoogle Scholar
  122. 122.
    Healy, B., & Cotter, P. D. (2017). 4 Lantibiotics: Bioengineering and applications. In Antimicrobial peptides: discovery, design and novel therapeutic strategies (2nd ed.). Wallingford, Oxfordshire, UK; Boston, MA: CABI.Google Scholar
  123. 123.
    Carroll, J., Field, D., O’ Connor, P. M., Cotter, P. D., Coffey, A., Hill, C., & O’Mahony, J. (2010). The gene encoded antimicrobial peptides, a template for the design of novel anti-mycobacterial drugs. Bioengineered Bugs, 1, 408–412.CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Field, D., Connor, P. M. O., Cotter, P. D., Hill, C., & Ross, R. P. (2008). The generation of nisin variants with enhanced activity against specific Gram-positive pathogens. Molecular Microbiology, 69, 218–230.CrossRefPubMedGoogle Scholar
  125. 125.
    Rouse, S., Field, D., Daly, K. M., O’Connor, P. M., Cotter, P. D., Hill, C., & Ross, R. P. (2012). Bioengineered nisin derivatives with enhanced activity in complex matrices. Microbial Biotechnology, 5, 501–508.CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Field, D., Quigley, L., O’Connor, P. M., Rea, M. C., Daly, K., Cotter, P. D., Hill, C., & Ross, R. P. (2010). Studies with bioengineered Nisin peptides highlight the broad-spectrum potency of Nisin V. Microbial Biotechnology, 3, 473–486.CrossRefPubMedPubMedCentralGoogle Scholar
  127. 127.
    Rihakova, J., Petit, V. W., Demnerova, K., Prévost, H., Rebuffat, S., & Drider, D. (2009). Insights into structure-activity relationships in the C-terminal region of divercin V41, a class IIa bacteriocin with high-level antilisterial activity. Applied and Environmental Microbiology, 75, 1811–1819.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Rihakova, J., Cappelier, J.-M., Hue, I., Demnerova, K., Fédérighi, M., Prévost, H., & Drider, D. (2010). In vivo activities of recombinant divercin V41 and its structural variants against Listeria monocytogenes. Antimicrobial Agents and Chemotherapy, 54, 563–564.CrossRefPubMedGoogle Scholar
  129. 129.
    Field, D., Gaudin, N., Lyons, F., O’Connor, P. M., Cotter, P. D., Hill, C., & Ross, R. P. (2015) A bioengineered nisin derivative to control biofilms of Staphylococcus pseudintermedius. PLoS ONE 10, e0119684.CrossRefPubMedPubMedCentralGoogle Scholar
  130. 130.
    Field, D., O’ Connor, R., Cotter, P. D., Ross, R. P., & Hill, C. (2016) In vitro activities of nisin and nisin derivatives alone and in combination with antibiotics against Staphylococcus biofilms. Frontiers in Microbiology, 7, 508.PubMedPubMedCentralGoogle Scholar
  131. 131.
    Brötz, H., & Sahl, H.-G. (2000). New insights into the mechanism of action of lantibiotics—diverse biological effects by binding to the same molecular target. Journal of Antimicrobial Chemotherapy, 46, 1–6.CrossRefPubMedGoogle Scholar
  132. 132.
    Gálvez, A., Maqueda, M., Martínez-Bueno, M., & Valdivia, E. (1991). Permeation of bacterial cells, permeation of cytoplasmic and artificial membrane vesicles, and channel formation on lipid bilayers by peptide antibiotic AS-48. Journal of Bacteriology, 173, 886–892.CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Zhao, T., Doyle, M. P., & Zhao, P. (2004). Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Applied and Environmental Microbiology, 70, 3996–4003.CrossRefPubMedPubMedCentralGoogle Scholar
  134. 134.
    Zhao, T., Podtburg, T. C., Zhao, P., Chen, D., Baker, D. A., Cords, B., & Doyle, M. P. (2013). Reduction by competitive bacteria of Listeria monocytogenes in biofilms and Listeria bacteria in floor drains in a ready-to-eat poultry processing plant. Journal of Food Protection, 76, 601–607.CrossRefPubMedGoogle Scholar
  135. 135.
    Schöbitz, R., González, C., Villarreal, K., Horzella, M., Nahuelquín, Y., & Fuentes, R. (2014). A biocontroller to eliminate Listeria monocytogenes from the food processing environment. Food Control, 36, 217–223.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departamento de VeterináriaUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Departamento de Alimentos e Nutrição ExperimentalUniversidade de São PauloSão PauloBrazil
  3. 3.Lille University, 7394–ICV-Institut Charles ViolletteLilleFrance
  4. 4.Lille University, CNRS, INRA, UMR 8207-UMET-PIHMVilleneuve d’AscqFrance

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