1887

Abstract

Bacteriocins are prokaryotic proteins or peptides with antimicrobial activity. Most of them exhibit a broad spectrum of activity, inhibiting micro-organisms belonging to different genera and species, including many bacterial pathogens which cause human, animal or plant infections. Therefore, these substances have potential biotechnological applications in either food preservation or prevention and control of bacterial infectious diseases. However, there is concern that continuous exposure of bacteria to bacteriocins may select cells resistant to them, as observed for conventional antimicrobials. Based on the models already investigated, bacteriocin resistance may be either innate or acquired and seems to be a complex phenomenon, arising at different frequencies (generally from 10 to 10) and by different mechanisms, even amongst strains of the same bacterial species. In the present review, we discuss the prevalence, development and molecular mechanisms involved in resistance to bacteriocins produced by Gram-positive bacteria. These mechanisms generally involve changes in the bacterial cell envelope, which result in (i) reduction or loss of bacteriocin binding or insertion, (ii) bacteriocin sequestering, (iii) bacteriocin efflux pumping (export) and (iv) bacteriocin degradation, amongst others. Strategies that can be used to overcome this resistance are also addressed.

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2015-04-01
2020-01-29
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References

  1. Abi Khattar Z., Rejasse A., Destoumieux-Garzón D., Escoubas J. M., Sanchis V., Lereclus D., Givaudan A., Kallassy M., Nielsen-Leroux C., Gaudriault S.. ( 2009;). The dlt operon of Bacillus cereus is required for resistance to cationic antimicrobial peptides and for virulence in insects. . J Bacteriol 191:, 7063–7073. [CrossRef][PubMed]
    [Google Scholar]
  2. Bastos M. C. F., Ceotto H.. ( 2011;). Bacterial antimicrobial peptides and food preservation. . In Natural Antimicrobials in Food Safety and Quality, pp. 62–76. Edited by Ray M., Chikindas M... Wallingford:: CAB International;. [CrossRef]
    [Google Scholar]
  3. Bastos M. C. F., Ceotto H., Coelho M. L. V., Nascimento J. S.. ( 2009;). Staphylococcal antimicrobial peptides: relevant properties and potential biotechnological applications. . Curr Pharm Biotechnol 10:, 38–61. [CrossRef][PubMed]
    [Google Scholar]
  4. Bastos M. C. F., Coutinho B. G., Coelho M. L. V.. ( 2010;). Lysostaphin: a staphylococcal bacteriolysin with potential clinical applications. . Pharmaceuticals (Basel) 3:, 1139–1161. [CrossRef]
    [Google Scholar]
  5. Begley M., Hill C., Ross R. P.. ( 2006;). Tolerance of Listeria monocytogenes to cell envelope-acting antimicrobial agents is dependent on SigB. . Appl Environ Microbiol 72:, 2231–2234. [CrossRef][PubMed]
    [Google Scholar]
  6. Begley M., Cotter P. D., Hill C., Ross R. P.. ( 2010;). Glutamate decarboxylase-mediated nisin resistance in Listeria monocytogenes. . Appl Environ Microbiol 76:, 6541–6546. [CrossRef][PubMed]
    [Google Scholar]
  7. Bergholz T. M., Tang S., Wiedmann M., Boor K. J.. ( 2013;). Nisin resistance of Listeria monocytogenes is increased by exposure to salt stress and is mediated via LiaR. . Appl Environ Microbiol 79:, 5682–5688. [CrossRef][PubMed]
    [Google Scholar]
  8. Bierbaum G., Sahl H.-G.. ( 2009;). Lantibiotics: mode of action, biosynthesis and bioengineering. . Curr Pharm Biotechnol 10:, 2–18. [CrossRef][PubMed]
    [Google Scholar]
  9. Blake K. L., Randall C. P., O’Neill A. J.. ( 2011;). In vitro studies indicate a high resistance potential for the lantibiotic nisin in Staphylococcus aureus and define a genetic basis for nisin resistance. . Antimicrob Agents Chemother 55:, 2362–2368. [CrossRef][PubMed]
    [Google Scholar]
  10. Bouttefroy A., Millière J.-B.. ( 2000;). Nisin-curvaticin 13 combinations for avoiding the regrowth of bacteriocin resistant cells of Listeria monocytogenes ATCC 15313. . Int J Food Microbiol 62:, 65–75. [CrossRef][PubMed]
    [Google Scholar]
  11. Breukink E., Wiedemann I., van Kraaij C., 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. [CrossRef][PubMed]
    [Google Scholar]
  12. Breukink E., van Heusden H. E., Vollmerhaus P. J., Swiezewska E., Brunner L., Walker S., Heck A. J., de Kruijff B.. ( 2003;). Lipid II is an intrinsic component of the pore induced by nisin in bacterial membranes. . J Biol Chem 278:, 19898–19903. [CrossRef][PubMed]
    [Google Scholar]
  13. Brötz H., Bierbaum G., Markus A., Molitor E., Sahl H.-G.. ( 1995;). Mode of action of the lantibiotic mersacidin: inhibition of peptidoglycan biosynthesis via a novel mechanism?. Antimicrob Agents Chemother 39:, 714–719. [CrossRef][PubMed]
    [Google Scholar]
  14. 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. . Mol Microbiol 30:, 317–327. [CrossRef][PubMed]
    [Google Scholar]
  15. Browder H. P., Zygmunt W. A., Young J. R., Tavormina P. A.. ( 1965;). Lysostaphin: enzymatic mode of action. . Biochem Biophys Res Commun 19:, 383–389. [CrossRef][PubMed]
    [Google Scholar]
  16. Bruno M. E. C., Montville T. J.. ( 1993;). Common mechanistic action of bacteriocins from lactic acid bacteria. . Appl Environ Microbiol 59:, 3003–3010.[PubMed]
    [Google Scholar]
  17. Butcher B. G., Helmann J. D.. ( 2006;). Identification of Bacillus subtilis σW-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. . Mol Microbiol 60:, 765–782. [CrossRef][PubMed]
    [Google Scholar]
  18. Cao M., Helmann J. D.. ( 2004;). The Bacillus subtilis extracytoplasmic-function σX factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. . J Bacteriol 186:, 1136–1146. [CrossRef][PubMed]
    [Google Scholar]
  19. Ceotto H., Holo H., da Costa K. F., Nascimento J. S., Salehian Z., Nes I. F., Bastos M. C. F.. ( 2010;). Nukacin 3299, a lantibiotic produced by Staphylococcus simulans 3299 identical to nukacin ISK-1. . Vet Microbiol 146:, 124–131. [CrossRef][PubMed]
    [Google Scholar]
  20. Climo M. W., Ehlert K., Archer G. L.. ( 2001;). Mechanism and suppression of lysostaphin resistance in oxacillin-resistant Staphylococcus aureus. . Antimicrob Agents Chemother 45:, 1431–1437. [CrossRef][PubMed]
    [Google Scholar]
  21. Coakley M., Fitzgerald G. F., Ros R. P.. ( 1997;). Application and evaluation of the phage resistance- and bacteriocin-encoding plasmid pMRC01 for the improvement of dairy starter cultures. . Appl Environ Microbiol 63:, 1434–1440.[PubMed]
    [Google Scholar]
  22. Coelho M. L. V., Nascimento J. S., Fagundes P. C., Madureira D. J., Oliveira S. S., Brito M. A. V. P., Bastos M. C. F.. ( 2007;). Activity of staphylococcal bacteriocins against Staphylococcus aureus and Streptococcus agalactiae involved in bovine mastitis. . Res Microbiol 158:, 625–630. [CrossRef][PubMed]
    [Google Scholar]
  23. Coelho M. L. V., Coutinho B. G., Santos O. C. S., Nes I. F., Bastos M. C. F.. ( 2014;). Immunity to the Staphylococcus aureus leaderless four-peptide bacteriocin aureocin A70 is conferred by AurI, an integral membrane protein. . Res Microbiol 165:, 50–59. [CrossRef][PubMed]
    [Google Scholar]
  24. Collins B., Curtis N., Cotter P. D., Hill C., Ross R. P.. ( 2010;a). The ABC transporter AnrAB contributes to the innate resistance of Listeria monocytogenes to nisin, bacitracin, and various beta-lactam antibiotics. . Antimicrob Agents Chemother 54:, 4416–4423. [CrossRef][PubMed]
    [Google Scholar]
  25. Collins B., Joyce S., Hill C., Cotter P. D., Ross R. P.. ( 2010;b). TelA contributes to the innate resistance of Listeria monocytogenes to nisin and other cell wall-acting antibiotics. . Antimicrob Agents Chemother 54:, 4658–4663. [CrossRef][PubMed]
    [Google Scholar]
  26. Collins B., Guinane C. M., Cotter P. D., Hill C., Ross R. P.. ( 2012;). Assessing the contributions of the LiaS histidine kinase to the innate resistance of Listeria monocytogenes to nisin, cephalosporins, and disinfectants. . Appl Environ Microbiol 78:, 2923–2929. [CrossRef][PubMed]
    [Google Scholar]
  27. Cotter P. D., Guinane C. M., Hill C.. ( 2002;). The LisRK signal transduction system determines the sensitivity of Listeria monocytogenes to nisin and cephalosporins. . Antimicrob Agents Chemother 46:, 2784–2790. [CrossRef][PubMed]
    [Google Scholar]
  28. Cotter P. D., Hill C., Ross R. P.. ( 2005;). Bacteriocins: developing innate immunity for food. . Nat Rev Microbiol 3:, 777–788. [CrossRef][PubMed]
    [Google Scholar]
  29. Cotter P. D., Ross R. P., Hill C.. ( 2013;). Bacteriocins – a viable alternative to antibiotics?. Nat Rev Microbiol 11:, 95–105. [CrossRef][PubMed]
    [Google Scholar]
  30. Crandall A. D., Montville T. J.. ( 1998;). Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. . Appl Environ Microbiol 64:, 231–237.[PubMed]
    [Google Scholar]
  31. Dalet K., Briand C., Cenatiempo Y., Héchard Y.. ( 2000;). The rpoN gene of Enterococcus faecalis directs sensitivity to subclass IIa bacteriocins. . Curr Microbiol 41:, 441–443. [CrossRef][PubMed]
    [Google Scholar]
  32. Dalet K., Cenatiempo Y., Cossart P., Héchard Y..European Listeria Genome Consortium ( 2001;). A σ54-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. . Microbiology 147:, 3263–3269.[PubMed]
    [Google Scholar]
  33. de Martinis E. C. P., Crandall A. D., Mazzotta A. S., Montville T. J.. ( 1997;). Influence of pH, salt, and temperature on nisin resistance in Listeria monocytogenes. . J Food Prot 60:, 420–423.
    [Google Scholar]
  34. Diep D. B., Skaugen M., Salehian Z., Holo H., Nes I. F.. ( 2007;). Common mechanisms of target cell recognition and immunity for class II bacteriocins. . Proc Natl Acad Sci U S A 104:, 2384–2389. [CrossRef][PubMed]
    [Google Scholar]
  35. Draper L. A., Grainger K., Deegan L. H., Cotter P. D., Hill C., Ross R. P.. ( 2009;). Cross-immunity and immune mimicry as mechanisms of resistance to the lantibiotic lacticin 3147. . Mol Microbiol 71:, 1043–1054. [CrossRef][PubMed]
    [Google Scholar]
  36. Draper L. A., Tagg J. R., Hill C., Cotter P. D., Ross R. P.. ( 2012;). The spiFEG locus in Streptococcus infantarius subsp. infantarius BAA-102 confers protection against nisin U. . Antimicrob Agents Chemother 56:, 573–578. [CrossRef][PubMed]
    [Google Scholar]
  37. Dubois J.-Y. F., Kouwen T. R. H. M., Schurich A. K., Reis C. R., Ensing H. T., Trip E. N., Zweers J. C., van Dijl J. M.. ( 2009;). Immunity to the bacteriocin sublancin 168 is determined by the SunI (YolF) protein of Bacillus subtilis. . Antimicrob Agents Chemother 53:, 651–661. [CrossRef][PubMed]
    [Google Scholar]
  38. Dykes G. A., Hastings J. W.. ( 1998;). Fitness costs associated with class IIa bacteriocin resistance in Listeria monocytogenes B73. . Lett Appl Microbiol 26:, 5–8. [CrossRef][PubMed]
    [Google Scholar]
  39. Ehlert K., Tschierske M., Mori C., Schröder W., Berger-Bächi B.. ( 2000;). Site-specific serine incorporation by Lif and Epr into positions 3 and 5 of the Staphylococcal peptidoglycan interpeptide bridge. . J Bacteriol 182:, 2635–2638. [CrossRef][PubMed]
    [Google Scholar]
  40. Fagundes, P. C. (2014). Characterization of hyicin 3682 and its potential application in the control of a phytopathogen. PhD thesis, Federal University of Rio de Janeiro, Brazil.
  41. Falord M., Mäder U., Hiron A., Débarbouillé M., Msadek T.. ( 2011;). Investigation of the Staphylococcus aureus GraSR regulon reveals novel links to virulence, stress response and cell wall signal transduction pathways. . PLoS ONE 6:, e21323. [CrossRef][PubMed]
    [Google Scholar]
  42. Fimland G., Eijsink V. G., Nissen-Meyer J.. ( 2002;). Comparative studies of immunity proteins of pediocin-like bacteriocins. . Microbiology 148:, 3661–3670.[PubMed]
    [Google Scholar]
  43. Fischer W.. ( 1988;). Physiology of lipoteichoic acids in bacteria. . Adv Microb Physiol 29:, 233–302. [CrossRef][PubMed]
    [Google Scholar]
  44. Freitag N. E., Port G. C., Miner M. D.. ( 2009;). Listeria monocytogenes – from saprophyte to intracellular pathogen. . Nat Rev Microbiol 7:, 623–628. [CrossRef][PubMed]
    [Google Scholar]
  45. Fritsch F., Mauder N., Williams T., Weiser J., Oberle M., Beier D.. ( 2011;). The cell envelope stress response mediated by the LiaFSRLm three-component system of Listeria monocytogenes is controlled via the phosphatase activity of the bifunctional histidine kinase LiaSLm. . Microbiology 157:, 373–386. [CrossRef][PubMed]
    [Google Scholar]
  46. Gabrielsen C., Brede D. A., Hernández P. E., Nes I. F., Diep D. B.. ( 2012;). The maltose ABC transporter in Lactococcus lactis facilitates high-level sensitivity to the circular bacteriocin garvicin ML. . Antimicrob Agents Chemother 56:, 2908–2915. [CrossRef][PubMed]
    [Google Scholar]
  47. Gajic O., Buist G., Kojic M., Topisirovic L., Kuipers O. P., Kok J.. ( 2003;). Novel mechanism of bacteriocin secretion and immunity carried out by lactococcal multidrug resistance proteins. . J Biol Chem 278:, 34291–34298. [CrossRef][PubMed]
    [Google Scholar]
  48. Gálvez A., Abriouel H., López R. L., Ben Omar N.. ( 2007;). Bacteriocin-based strategies for food biopreservation. . Int J Food Microbiol 120:, 51–70. [CrossRef][PubMed]
    [Google Scholar]
  49. Gargis S. R., Heath H. E., LeBlanc P. A., Dekker L., Simmonds R. S., Sloan G. L.. ( 2010;). Inhibition of the activity of both domains of lysostaphin through peptidoglycan modification by the lysostaphin immunity protein. . Appl Environ Microbiol 76:, 6944–6946. [CrossRef][PubMed]
    [Google Scholar]
  50. Grande Burgos M. J., Kovács A. T., Mirończuk A. M., Abriouel H., Gálvez A., Kuipers O. P.. ( 2009;). Response of Bacillus cereus ATCC 14579 to challenges with sublethal concentrations of enterocin AS-48. . BMC Microbiol 9:, 227–234. [CrossRef][PubMed]
    [Google Scholar]
  51. Gravesen A., Sørensen K., Aarestrup F. M., Knøchel S.. ( 2001;). Spontaneous nisin-resistant Listeria monocytogenes mutants with increased expression of a putative penicillin-binding protein and their sensitivity to various antibiotics. . Microb Drug Resist 7:, 127–135. [CrossRef][PubMed]
    [Google Scholar]
  52. Gravesen A., Jydegaard Axelsen A. M., Mendes da Silva J., Hansen T. B., Knøchel S.. ( 2002;a). Frequency of bacteriocin resistance development and associated fitness costs in Listeria monocytogenes. . Appl Environ Microbiol 68:, 756–764. [CrossRef][PubMed]
    [Google Scholar]
  53. Gravesen A., Ramnath M., Rechinger K. B., Andersen N., Jänsch L., Héchard Y., Hastings J. W., Knøchel S.. ( 2002;b). High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. . Microbiology 148:, 2361–2369.[PubMed]
    [Google Scholar]
  54. Gravesen A., Kallipolitis B., Holmstrøm K., Høiby P. E., Ramnath M., Knøchel S.. ( 2004;). pbp2229-mediated nisin resistance mechanism in Listeria monocytogenes confers cross-protection to class IIa bacteriocins and affects virulence gene expression. . Appl Environ Microbiol 70:, 1669–1679. [CrossRef][PubMed]
    [Google Scholar]
  55. Guignard B., Entenza J. M., Moreillon P.. ( 2005;). Beta-lactams against methicillin-resistant Staphylococcus aureus. . Curr Opin Pharmacol 5:, 479–489. [CrossRef][PubMed]
    [Google Scholar]
  56. Guinane C. M., Cotter P. D., Hill C., Ross R. P.. ( 2006;). Spontaneous resistance in Lactococcus lactis IL1403 to the lantibiotic lacticin 3147. . FEMS Microbiol Lett 260:, 77–83. [CrossRef][PubMed]
    [Google Scholar]
  57. Héchard Y., Pelletier C., Cenatiempo Y., Frère J.. ( 2001;). Analysis of σ54-dependent genes in Enterococcus faecalis: a mannose PTS permease (EIIMan) is involved in sensitivity to a bacteriocin, mesentericin Y105. . Microbiology 147:, 1575–1580.[PubMed]
    [Google Scholar]
  58. Heidrich C., Pag U., Josten M., Metzger J., Jack R. W., Bierbaum G., Jung G., Sahl H.-G.. ( 1998;). Isolation, characterization, and heterologous expression of the novel lantibiotic epicidin 280 and analysis of its biosynthetic gene cluster. . Appl Environ Microbiol 64:, 3140–3146.[PubMed]
    [Google Scholar]
  59. 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 Bacteriocins: Ecology and Evolution, pp. 45–92. Edited by Riley M. A., Chavan M. A... New York:: Springer;. [CrossRef]
    [Google Scholar]
  60. Hillman J. D., Mo J., McDonell E., Cvitkovitch D., Hillman C. H.. ( 2007;). Modification of an effector strain for replacement therapy of dental caries to enable clinical safety trials. . J Appl Microbiol 102:, 1209–1219. [CrossRef][PubMed]
    [Google Scholar]
  61. Hiron A., Falord M., Valle J., Débarbouillé M., Msadek T.. ( 2011;). Bacitracin and nisin resistance in Staphylococcus aureus: a novel pathway involving the BraS/BraR two-component system (SA2417/SA2418) and both the BraD/BraE and VraD/VraE ABC transporters. . Mol Microbiol 81:, 602–622. [CrossRef][PubMed]
    [Google Scholar]
  62. Hoffmann A., Schneider T., Pag U., Sahl H.-G.. ( 2004;). Localization and functional analysis of PepI, the immunity peptide of Pep5-producing Staphylococcus epidermidis strain 5. . Appl Environ Microbiol 70:, 3263–3271. [CrossRef][PubMed]
    [Google Scholar]
  63. Islam M. R., Nishie M., Nagao J., Zendo T., Keller S., Nakayama J., Kohda D., Sahl H.-G., Sonomoto K.. ( 2012;). Ring A of nukacin ISK-1: a lipid II-binding motif for type-A(II) lantibiotic. . J Am Chem Soc 134:, 3687–3690. [CrossRef][PubMed]
    [Google Scholar]
  64. Jack R. W., Tagg J. R., Ray B.. ( 1995;). Bacteriocins of gram-positive bacteria. . Microbiol Rev 59:, 171–200.[PubMed]
    [Google Scholar]
  65. Jarvis B.. ( 1967;). Resistance to nisin and production of nisin-inactivating enzymes by several Bacillus species. . J Gen Microbiol 47:, 33–48. [CrossRef][PubMed]
    [Google Scholar]
  66. Jarvis B., Farr J.. ( 1971;). Partial purification, specificity and mechanism of action of the nisin-inactivating enzyme from Bacillus cereus. . Biochim Biophys Acta 227:, 232–240. [CrossRef][PubMed]
    [Google Scholar]
  67. Jydegaard A. M., Gravesen A., Knøchel S.. ( 2000;). Growth condition-related response of Listeria monocytogenes 412 to bacteriocin inactivation. . Lett Appl Microbiol 31:, 68–72. [CrossRef][PubMed]
    [Google Scholar]
  68. Katla T., Møretrø T., Sveen I., Aasen I. M., Axelsson L., Rørvik L. M., Naterstad K.. ( 2002;). Inhibition of Listeria monocytogenes in chicken cold cuts by addition of sakacin P and sakacin P-producing Lactobacillus sakei. . J Appl Microbiol 93:, 191–196. [CrossRef][PubMed]
    [Google Scholar]
  69. Katla T., Naterstad K., Vancanneyt M., Swings J., Axelsson L.. ( 2003;). Differences in susceptibility of Listeria monocytogenes strains to sakacin P, sakacin A, pediocin PA-1, and nisin. . Appl Environ Microbiol 69:, 4431–4437. [CrossRef][PubMed]
    [Google Scholar]
  70. Kaur G., Singh T. P., Malik R. K.. ( 2013;). Antibacterial efficacy of Nisin, Pediocin 34 and Enterocin FH99 against Listeria monocytogenes and cross resistance of its bacteriocin resistant variants to common food preservatives. . Braz J Microbiol 44:, 63–71. [CrossRef][PubMed]
    [Google Scholar]
  71. Kawada-Matsuo M., Yoshida Y., Zendo T., Nagao J., Oogai Y., Nakamura Y., Sonomoto K., Nakamura N., Komatsuzawa H.. ( 2013;a). Three distinct two-component systems are involved in resistance to the class I bacteriocins, nukacin ISK-1 and nisin A, in Staphylococcus aureus. . PLoS ONE 8:, e69455. [CrossRef][PubMed]
    [Google Scholar]
  72. Kawada-Matsuo M., Oogai Y., Zendo T., Nagao J., Shibata Y., Yamashita Y., Ogura Y., Hayashi T., Sonomoto K., Komatsuzawa H.. ( 2013;b). Involvement of the novel two-component NsrRS and LcrRS systems in distinct resistance pathways against nisin A and nukacin ISK-1 in Streptococcus mutans. . Appl Environ Microbiol 79:, 4751–4755. [CrossRef][PubMed]
    [Google Scholar]
  73. Kingston A. W., Liao X., Helmann J. D.. ( 2013;). Contributions of the σW, σM and σX regulons to the lantibiotic resistome of Bacillus subtilis. . Mol Microbiol 90:, 502–518. [CrossRef][PubMed]
    [Google Scholar]
  74. Kiri N., Archer G., Climo M. W.. ( 2002;). Combinations of lysostaphin with β-lactams are synergistic against oxacillin-resistant Staphylococcus epidermidis. . Antimicrob Agents Chemother 46:, 2017–2020. [CrossRef][PubMed]
    [Google Scholar]
  75. Kjos M., Snipen L., Salehian Z., Nes I. F., Diep D. B.. ( 2010;a). The Abi proteins and their involvement in bacteriocin self-immunity. . J Bacteriol 192:, 2068–2076. [CrossRef][PubMed]
    [Google Scholar]
  76. Kjos M., Salehian Z., Nes I. F., Diep D. B.. ( 2010;b). An extracellular loop of the mannose phosphotransferase system component IIC is responsible for specific targeting by class IIa bacteriocins. . J Bacteriol 192:, 5906–5913. [CrossRef][PubMed]
    [Google Scholar]
  77. Kjos M., Nes I. F., Diep D. B.. ( 2011;). Mechanisms of resistance to bacteriocins targeting the mannose phosphotransferase system. . Appl Environ Microbiol 77:, 3335–3342. [CrossRef][PubMed]
    [Google Scholar]
  78. Kramer N. E., Hasper H. E., van den Bogaard P. T. C., Morath S., de Kruijff B., Hartung T., Smid E. J., Breukink E., Kok J., Kuipers O. P.. ( 2008;). Increased d-alanylation of lipoteichoic acid and a thickened septum are main determinants in the nisin resistance mechanism of Lactococcus lactis. . Microbiology 154:, 1755–1762. [CrossRef][PubMed]
    [Google Scholar]
  79. Kusuma C. M., Kokai-Kun J. F.. ( 2005;). Comparison of four methods for determining lysostaphin susceptibility of various strains of Staphylococcus aureus. . Antimicrob Agents Chemother 49:, 3256–3263. [CrossRef][PubMed]
    [Google Scholar]
  80. Kusuma C. M., Jadanova A., Chanturiya T., Kokai-Kun J. F.. ( 2007;). Lysostaphin-resistant variants of Staphylococcus aureus demonstrate reduced fitness in vitro and in vivo. . Antimicrob Agents Chemother 51:, 475–482. [CrossRef][PubMed]
    [Google Scholar]
  81. Laursen M. F., Bahl M. I., Licht T. R., Gram L., Knudsen G. M.. ( 2014;). A single exposure to a sublethal pediocin concentration initiates a resistance-associated temporal cell envelope and general stress response in Listeria monocytogenes. . Environ Microbiol n/a. [CrossRef][PubMed]
    [Google Scholar]
  82. Limonet M., Revol-Junelles A. M., Millière J. B.. ( 2002;). Variations in the membrane fatty acid composition of resistant or susceptible Leuconostoc or Weissella strains in the presence or absence of Mesenterocin 52A and Mesenterocin 52B produced by Leuconostoc mesenteroides subsp. mesenteroides FR52. . Appl Environ Microbiol 68:, 2910–2916. [CrossRef][PubMed]
    [Google Scholar]
  83. Macwana S., Muriana P. M.. ( 2012;). Spontaneous bacteriocin resistance in Listeria monocytogenes as a susceptibility screen for identifying different mechanisms of resistance and modes of action by bacteriocins of lactic acid bacteria. . J Microbiol Methods 88:, 7–13. [CrossRef][PubMed]
    [Google Scholar]
  84. Maisnier-Patin S., Richard J.. ( 1996;). Cell wall changes in nisin-resistant variants of Listeria innocua grown in the presence of high nisin concentrations. . FEMS Microbiol Lett 140:, 29–35. [CrossRef][PubMed]
    [Google Scholar]
  85. Mandin P., Fsihi H., Dussurget O., Vergassola M., Milohanic E., Toledo-Arana A., Lasa I., Johansson J., Cossart P.. ( 2005;). VirR, a response regulator critical for Listeria monocytogenes virulence. . Mol Microbiol 57:, 1367–1380. [CrossRef][PubMed]
    [Google Scholar]
  86. Mantovani H. C., Russell J. B.. ( 2001;). Nisin resistance of Streptococcus bovis. . Appl Environ Microbiol 67:, 808–813. [CrossRef][PubMed]
    [Google Scholar]
  87. Martínez B., Rodríguez A., Suárez J. E.. ( 2000;). Lactococcin 972, a bacteriocin that inhibits septum formation in lactococci. . Microbiology 146:, 949–955.[PubMed]
    [Google Scholar]
  88. Mascher T., Zimmer S. L., Smith T.-A., Helmann J. D.. ( 2004;). Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. . Antimicrob Agents Chemother 48:, 2888–2896. [CrossRef][PubMed]
    [Google Scholar]
  89. Mazzotta A. S., Crandall A. D., Montville T. J.. ( 1997;). Nisin resistance in Clostridium botulinum spores and vegetative cells. . Appl Environ Microbiol 63:, 2654–2659.[PubMed]
    [Google Scholar]
  90. McBride S. M., Sonenshein A. L.. ( 2011;a). The dlt operon confers resistance to cationic antimicrobial peptides in Clostridium difficile. . Microbiology 157:, 1457–1465. [CrossRef][PubMed]
    [Google Scholar]
  91. McBride S. M., Sonenshein A. L.. ( 2011;b). Identification of a genetic locus responsible for antimicrobial peptide resistance in Clostridium difficile. . Infect Immun 79:, 167–176. [CrossRef][PubMed]
    [Google Scholar]
  92. Mendoza F., Maqueda M., Gálvez A., Martínez-Bueno M., Valdivia E.. ( 1999;). Antilisterial activity of peptide AS-48 and study of changes induced in the cell envelope properties of an AS-48-adapted strain of Listeria monocytogenes. . Appl Environ Microbiol 65:, 618–625.[PubMed]
    [Google Scholar]
  93. Ming X., Daeschel M. A.. ( 1993;). Nisin resistance of foodborne bacteria and the specific resistance responses of Listeria monocytogenes Scott A. . J Food Prot 56:, 944–948.
    [Google Scholar]
  94. Naghmouchi K., Kheadr E., Lacroix C., Fliss I.. ( 2007;). Class I/Class IIa bacteriocin cross-resistance phenomenon in Listeria monocytogenes. . Food Microbiol 24:, 718–727. [CrossRef][PubMed]
    [Google Scholar]
  95. Nascimento J. S., Coelho M. L. V., Ceotto H., Potter A., Fleming L. R., Salehian Z., Nes I. F., Bastos M. C. F.. ( 2012;). Genes involved in immunity to and secretion of aureocin A53, an atypical class II bacteriocin produced by Staphylococcus aureus A53. . J Bacteriol 194:, 875–883. [CrossRef][PubMed]
    [Google Scholar]
  96. Nes I. F., Yoon S.-S., Diep D. B.. ( 2007;). Ribosomally synthesized antimicrobial peptides (bacteriocins) in lactic acid bacteria: a review. . Food Sci Biotechnol 16:, 675–690.
    [Google Scholar]
  97. Netz D. J. A., Bastos M. C. F., Sahl H.-G.. ( 2002;). Mode of action of the antimicrobial peptide aureocin A53 from Staphylococcus aureus. . Appl Environ Microbiol 68:, 5274–5280. [CrossRef][PubMed]
    [Google Scholar]
  98. Nissen-Meyer J., Rogne P., Oppegård C., Haugen H. S., Kristiansen P. E.. ( 2009;). Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by gram-positive bacteria. . Curr Pharm Biotechnol 10:, 19–37. [CrossRef][PubMed]
    [Google Scholar]
  99. Oppegård C., Emanuelsen L., Thorbek L., Fimland G., Nissen-Meyer J.. ( 2010;). The lactococcin G immunity protein recognizes specific regions in both peptides constituting the two-peptide bacteriocin lactococcin G. . Appl Environ Microbiol 76:, 1267–1273. [CrossRef][PubMed]
    [Google Scholar]
  100. Opsata M., Nes I. F., Holo H.. ( 2010;). Class IIa bacteriocin resistance in Enterococcus faecalis V583: the mannose PTS operon mediates global transcriptional responses. . BMC Microbiol 10:, 224. [CrossRef][PubMed]
    [Google Scholar]
  101. Palmer M. E., Wiedmann M., Boor K. J.. ( 2009;). σB and σL contribute to Listeria monocytogenes 10403S response to the antimicrobial peptides SdpC and nisin. . Foodborne Pathog Dis 6:, 1057–1065. [CrossRef][PubMed]
    [Google Scholar]
  102. Peschel A., Otto M., Jack R. W., Kalbacher H., Jung G., Götz F.. ( 1999;). Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. . J Biol Chem 274:, 8405–8410. [CrossRef][PubMed]
    [Google Scholar]
  103. Peschel A., Jack R. W., Otto M., Collins L. V., Staubitz P., Nicholson G., Kalbacher H., Nieuwenhuizen W. F., Jung G. et al. ( 2001;). Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. . J Exp Med 193:, 1067–1076. [CrossRef][PubMed]
    [Google Scholar]
  104. Postma P. W., Lengeler J. W., Jacobson G. R.. ( 1993;). Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. . Microbiol Rev 57:, 543–594.[PubMed]
    [Google Scholar]
  105. Potter A., Ceotto H., Coelho M. L. V., Guimarães A. J., Bastos M. C. F.. ( 2014;). The gene cluster of aureocyclicin 4185: the first cyclic bacteriocin of Staphylococcus aureus. . Microbiology 160:, 917–928. [CrossRef][PubMed]
    [Google Scholar]
  106. Ramnath M., Beukes M., Tamura K., Hastings J. W.. ( 2000;). Absence of a putative mannose-specific phosphotransferase system enzyme IIAB component in a leucocin A-resistant strain of Listeria monocytogenes, as shown by two-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis. . Appl Environ Microbiol 66:, 3098–3101. [CrossRef][PubMed]
    [Google Scholar]
  107. Ramnath M., Arous S., Gravesen A., Hastings J. W., Héchard Y.. ( 2004;). Expression of mptC of Listeria monocytogenes induces sensitivity to class IIa bacteriocins in Lactococcus lactis. . Microbiology 150:, 2663–2668. [CrossRef][PubMed]
    [Google Scholar]
  108. Rasch M., Knøchel S.. ( 1998;). Variations in tolerance of Listeria monocytogenes to nisin, pediocin PA-1 and bavaricin A. . Lett Appl Microbiol 27:, 275–278. [CrossRef][PubMed]
    [Google Scholar]
  109. Rekhif N., Atrih A., Lefebvre G.. ( 1994;). Selection and properties of spontaneous mutants of Listeria monocytogenes ATCC 15313 resistant to different bacteriocins produced by lactic acid bacteria strains. . Curr Microbiol 28:, 237–241. [CrossRef]
    [Google Scholar]
  110. Robichon D., Gouin E., Débarbouillé M., Cossart P., Cenatiempo Y., Héchard Y.. ( 1997;). The rpoN54) gene from Listeria monocytogenes is involved in resistance to mesentericin Y105, an antibacterial peptide from Leuconostoc mesenteroides. . J Bacteriol 179:, 7591–7594.[PubMed]
    [Google Scholar]
  111. Roces C., Courtin P., Kulakauskas S., Rodríguez A., Chapot-Chartier M. P., Martínez B.. ( 2012;a). Isolation of Lactococcus lactis mutants simultaneously resistant to the cell wall-active bacteriocin Lcn972, lysozyme, nisin, and bacteriophage c2. . Appl Environ Microbiol 78:, 4157–4163. [CrossRef][PubMed]
    [Google Scholar]
  112. Roces C., Pérez V., Campelo A. B., Blanco D., Kok J., Kuipers O. P., Rodríguez A., Martínez B.. ( 2012;b). The putative lactococcal extracytoplasmic function anti-sigma factor Llmg2447 determines resistance to the cell wall-active bacteriocin Lcn972. . Antimicrob Agents Chemother 56:, 5520–5527. [CrossRef][PubMed]
    [Google Scholar]
  113. Rohrer S., Berger-Bächi B.. ( 2003;). FemABX peptidyl transferases: a link between branched-chain cell wall peptide formation and β-lactam resistance in gram-positive cocci. . Antimicrob Agents Chemother 47:, 837–846. [CrossRef][PubMed]
    [Google Scholar]
  114. Ryan M. P., Meaney W. J., Ross R. P., Hill C.. ( 1998;). Evaluation of lacticin 3147 and a teat seal containing this bacteriocin for inhibition of mastitis pathogens. . Appl Environ Microbiol 64:, 2287–2290.[PubMed]
    [Google Scholar]
  115. Ryan M. P., Flynn J., Hill C., Ross R. P., Meaney W. J.. ( 1999;). The natural food grade inhibitor, lacticin 3147, reduced the incidence of mastitis after experimental challenge with Streptococcus dysgalactiae in nonlactating dairy cows. . J Dairy Sci 82:, 2108–2114. [CrossRef][PubMed]
    [Google Scholar]
  116. Samant S., Hsu F. F., Neyfakh A. A., Lee H.. ( 2009;). The Bacillus anthracis protein MprF is required for synthesis of lysylphosphatidylglycerols and for resistance to cationic antimicrobial peptides. . J Bacteriol 191:, 1311–1319. [CrossRef][PubMed]
    [Google Scholar]
  117. Schindler C. A., Schuhardt V. T.. ( 1965;). Purification and properties of lysostaphin – a lytic agent for Staphylococcus aureus. . Biochim Biophys Acta 97:, 242–250. [CrossRef][PubMed]
    [Google Scholar]
  118. Strandén A. M., Ehlert K., Labischinski H., Berger-Bächi B.. ( 1997;). Cell wall monoglycine cross-bridges and methicillin hypersusceptibility in a femAB null mutant of methicillin-resistant Staphylococcus aureus. . J Bacteriol 179:, 9–16.[PubMed]
    [Google Scholar]
  119. Suda S., Cotter P. D., Hill C., Ross R. P.. ( 2012;). Lacticin 3147 – biosynthesis, molecular analysis, immunity, bioengineering and applications. . Curr Protein Pept Sci 13:, 193–204. [CrossRef][PubMed]
    [Google Scholar]
  120. Sun Z., Zhong J., Liang X., Liu J., Chen X., Huan L.. ( 2009;). Novel mechanism for nisin resistance via proteolytic degradation of nisin by the nisin resistance protein NSR. . Antimicrob Agents Chemother 53:, 1964–1973. [CrossRef][PubMed]
    [Google Scholar]
  121. Tessema G. T., Møretrø T., Kohler A., Axelsson L., Naterstad K.. ( 2009;). Complex phenotypic and genotypic responses of Listeria monocytogenes strains exposed to the class IIa bacteriocin sakacin P. . Appl Environ Microbiol 75:, 6973–6980. [CrossRef][PubMed]
    [Google Scholar]
  122. Tessema G. T., Møretrø T., Snipen L., Axelsson L., Naterstad K.. ( 2011;). Global transcriptional analysis of spontaneous sakacin P-resistant mutant strains of Listeria monocytogenes during growth on different sugars. . PLoS ONE 6:, e16192. [CrossRef][PubMed]
    [Google Scholar]
  123. Thedieck K., Hain T., Mohamed W., Tindall B. J., Nimtz M., Chakraborty T., Wehland J., Jänsch L.. ( 2006;). The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. . Mol Microbiol 62:, 1325–1339. [CrossRef][PubMed]
    [Google Scholar]
  124. Thumm G., Götz F.. ( 1997;). Studies on prolysostaphin processing and characterization of the lysostaphin immunity factor (Lif) of Staphylococcus simulans biovar staphylolyticus. . Mol Microbiol 23:, 1251–1265. [CrossRef][PubMed]
    [Google Scholar]
  125. Vadyvaloo V., Hastings J. W., van der Merwe M. J., Rautenbach M.. ( 2002;). Membranes of class IIa bacteriocin-resistant Listeria monocytogenes cells contain increased levels of desaturated and short-acyl-chain phosphatidylglycerols. . Appl Environ Microbiol 68:, 5223–5230. [CrossRef][PubMed]
    [Google Scholar]
  126. Vadyvaloo V., Arous S., Gravesen A., Héchard Y., Chauhan-Haubrock R., Hastings J. W., Rautenbach M.. ( 2004;). Cell-surface alterations in class IIa bacteriocin-resistant Listeria monocytogenes strains. . Microbiology 150:, 3025–3033. [CrossRef][PubMed]
    [Google Scholar]
  127. van Belkum M. J., Martin-Visscher L. A., Vederas J. C.. ( 2011;). Structure and genetics of circular bacteriocins. . Trends Microbiol 19:, 411–418. [CrossRef][PubMed]
    [Google Scholar]
  128. van Heusden H. E., de Kruijff B., Breukink E.. ( 2002;). Lipid II induces a transmembrane orientation of the pore-forming peptide lantibiotic nisin. . Biochemistry 41:, 12171–12178. [CrossRef][PubMed]
    [Google Scholar]
  129. van Schaik W., Gahan C. G., Hill C.. ( 1999;). Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin 3147. . J Food Prot 62:, 536–539.[PubMed]
    [Google Scholar]
  130. Verheul A., Russell N. J., Van’T Hof R., Rombouts F. M., Abee T.. ( 1997;). Modifications of membrane phospholipid composition in nisin-resistant Listeria monocytogenes Scott A. . Appl Environ Microbiol 63:, 3451–3457.[PubMed]
    [Google Scholar]
  131. Vignolo G., Palacios J., Farías 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. . Curr Microbiol 41:, 410–416. [CrossRef][PubMed]
    [Google Scholar]
  132. Wan J., Harmark K., Davidson B. E., Hillier A. J., Gordon J. B., Wilcock A., Hickey M. W., Coventry M. J.. ( 1997;). Inhibition of Listeria monocytogenes by piscicolin 126 in milk and Camembert cheese manufactured with a thermophilic starter. . J Appl Microbiol 82:, 273–280. [CrossRef][PubMed]
    [Google Scholar]
  133. Wiedemann I., Böttiger T., Bonelli R. R., Wiese A., Hagge S. O., Gutsmann T., Seydel U., Deegan L., Hill C. et al. ( 2006;). The mode of action of the lantibiotic lacticin 3147 – a complex mechanism involving specific interaction of two peptides and the cell wall precursor lipid II. . Mol Microbiol 61:, 285–296. [CrossRef][PubMed]
    [Google Scholar]
  134. Xuanyuan Z., Wu Z., Li R., Jiang D., Su J., Xu H., Bai Y., Zhang X., Saris P. E. J., Qiao M.. ( 2010;). Loss of IrpT function in Lactococcus lactis subsp. lactis N8 results in increased nisin resistance. . Curr Microbiol 61:, 329–334. [CrossRef][PubMed]
    [Google Scholar]
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