Skip to main content
Log in

Pediocin-Like Antimicrobial Peptides of Bacteria

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Bacteriocins are bacterial antimicrobial peptides that, unlike classical peptide antibiotics, are products of ribosomal synthesis and usually have a narrow spectrum of antibacterial activity against species closely related to the producers. Pediocin-like bacteriocins (PLBs) belong to the class IIa of the bacteriocins of Gram-positive bacteria. PLBs possess high activity against pathogenic bacteria from Listeria and Enterococcus genera. Molecular target for PLBs is a membrane protein complex — bacterial mannose-phosphotransferase. PLBs can be synthesized by components of symbiotic microflora and participate in the maintenance of homeostasis in various compartments of the digestive tract and on the surface of epithelial tissues contacting the external environment. PLBs could give a rise to a new group of antibiotics of narrow spectrum of activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

GI:

gastrointestinal (tract)

Man-PTS:

mannose phosphotransferase

MIC:

minimal inhibitory concentration

PLBs:

pediocin-like bacteriocins

PTS:

phosphoenolpyruvate:carbohydrate phosphotransferase system

References

  1. Cotter, P. D., Ross, R. P., and Hill, C. (2013) Bacteriocins — a viable alternative to antibiotics? Nat. Rev. Microbiol., 11, 95–105.

    Article  CAS  PubMed  Google Scholar 

  2. Kemperman, R., Kuipers, A., Karsens, H., Nauta, A., Kuipers, O., and Kok, J. (2003) Identification and characterization of two novel clostridial bacteriocins, circularin A and closticin 574, Appl. Environ. Microbiol., 69, 1589–1597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Svetoch, E. A., Eruslanov, B. V., Perelygin, V. V., Mitsevich, E. V., Mitsevich, I. P., Borzenkov, V. N., Levchuk, V. P., Svetoch, O. E., Kovalev, Y. N., Stepanshin, Y. G., Siragusa, G. R., Seal, B. S., and Stern, N. J. (2008) Diverse antimicrobial killing by Enterococcus faecium E 50–52 bacteriocin, J. Agric. Food Chem., 56, 1942–1948.

    Article  CAS  PubMed  Google Scholar 

  4. Cotter, P. D., Hill, C., and Ross, R. P. (2005) Bacteriocins: developing innate immunity for food, Nat. Rev. Microbiol., 3, 777–788.

    Article  CAS  PubMed  Google Scholar 

  5. Svetoch, E. A., and Stern, N. J. (2010) Bacteriocins to control Campylobacter spp. in poultry — a review, Poult. Sci., 89, 1763–1768.

    Article  CAS  PubMed  Google Scholar 

  6. Desriac, F., Defer, D., Bourgougnon, N., Brillet, B., Le Chevalier, P., and Fleury, Y. (2010) Bacteriocin as weapons in the marine animal-associated bacteria warfare: inventory and potential applications as an aquaculture probiotic, Mar. Drugs, 8, 1153–1177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Gharsallaoui, A., Oulahal, N., Joly, C., and Degraeve, P. (2016) Nisin as a food preservative. Part 1: Physicochemical properties, antimicrobial activity, and main uses, Crit. Rev. Food Sci. Nutr., 56, 1262–1274.

    Article  CAS  PubMed  Google Scholar 

  8. Shin, J. M., Gwak, J. W., Kamarajan, P., Fenno, J. C., Rickard, A. H., and Kapila, Y. L. (2016) Biomedical applications of nisin, J. Appl. Microbiol., 120, 1449–1465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Panteleev, P. V., Balandin, S. V., Ivanov, V. T., and Ovchinnikova, T. V. (2017) A therapeutic potential of animal β-hairpin antimicrobial peptides, Curr. Med. Chem., 24, 1724–1746.

    Article  CAS  PubMed  Google Scholar 

  10. Maxson, T, and Mitchell, D. A. (2016) Targeted treatment for bacterial infections: prospects for pathogen-specific antibiotics coupled with rapid diagnostics, Tetrahedron, 72, 3609–3624.

    Article  CAS  PubMed  Google Scholar 

  11. Melander, R. J., Zurawski, D. V., and Melander, C. (2018) Narrow-spectrum antibacterial agents, Medchemcomm, 9, 12–21.

    Article  CAS  PubMed  Google Scholar 

  12. Klaenhammer, T. R. (1993) Genetics of bacteriocins produced by lactic acid bacteria, FEMS Microbiol. Rev., 12, 39–85.

    Article  CAS  PubMed  Google Scholar 

  13. Drider, D., Fimland, G., Hechard, Y., McMullen, L. M., and Prevost, H. (2006) The continuing story of class IIa bacteriocins, Microbiol. Mol. Biol. Rev., 70, 564–582.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Papagianni, M., and Anastasiadou, S. (2009) Pediocins: the bacteriocins of pediococci. Sources, production, properties and applications, Microb. Cell Fact., 8, 3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Rhos Colombo, N. S., Chalon, M. C., Navarro, S. A., and Bellomio, A. (2018) Pediocin-like bacteriocins: new perspectives on mechanism of action and immunity, Curr. Genet., 64, 345–351.

    Article  CAS  Google Scholar 

  16. Bhunia, A. K., Johnson, M. C., and Ray, B. (1988) Purification, characterization and antimicrobial spectrum of a bacteriocin produced by Pediococcus acidilactici, J. Appl. Bacteriol., 65, 261–268.

    Article  CAS  PubMed  Google Scholar 

  17. Hastings, J. W., Sailer, M., Johnson, K., Roy, K. L., Vederas, J. C., and Stiles, M. E. (1991) Characterization of leucocin A-UAL 187 and cloning of the bacteriocin gene from Leuconostoc gelidum, J. Bacteriol., 173, 7491–7500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Motlagh, A. M., Bhunia, A. K., Szostek, F., Hansen, T. R., Johnson, M. C., and Ray, B. (1992) Nucleotide and amino acid sequence of pap-gene (pediocin AcH production) in Pediococcus acidilactici H, Lett. Appl. Microbiol., 15, 45–48.

    Article  CAS  PubMed  Google Scholar 

  19. Henderson, J. T., Chopko, A. L., and van Wassenaar, P. D. (1992) Purification and primary structure of pediocin PA-1 produced by Pediococcus acidilactici PAC-1.0, Arch. Biochem. Biophys., 295, 5–12.

    Article  CAS  PubMed  Google Scholar 

  20. Cui, Y., Zhang, C., Wang, Y., Shi, J., Zhang, L., Ding, Z., Qu, X., and Cui, H. (2012) Class IIa bacteriocins: diversity and new developments, Int. J. Mol. Sci., 13, 16668–16707.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Yildirim, Z., and Johnson, M. G. (1998) Characterization and antimicrobial spectrum of bifidocin B, a bacteriocin produced by Bifidobacterium bifidum NCFB 1454, J. Food Prot., 61, 47–51.

    Article  CAS  PubMed  Google Scholar 

  22. Cheikhyoussef, A., Cheikhyoussef, N., Chen, H., Zhao, J., Tang, J., Zhang, H., and Chen, W. (2010) Bifidin I — a new bacteriocin produced by Bifidobacterium infantis BCRC 14602: purification and partial amino acid sequence, Food Control, 21, 746–753.

    Article  CAS  Google Scholar 

  23. Le Marrec, C., Hyronimus, B., Bressollier, P., Verneuil, B., and Urdaci, M. C. (2000) Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I(4), Appl. Environ. Microbiol., 66, 5213–5220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kalmokoff, M. L., Banerjee, S. K., Cyr, T., Hefford, M. A., and Gleeson, T. (2001) Identification of a new plasmid-encoded Sec-dependent bacteriocin produced by Listeria innocua 743, Appl. Environ. Microbiol., 67, 4041–4047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Zheng, J., Ganzle, M. G., Lin, X. B., Ruan, L., and Sun, M. (2015) Diversity and dynamics of bacteriocins from human microbiome, Environ. Microbiol., 17, 2133–2143.

    Article  CAS  PubMed  Google Scholar 

  26. Cleveland, J., Montville, T. J., Nes, I. F., and Chikindas, M. L. (2001) Bacteriocins: safe, natural antimicrobials for food preservation, Int. J. Food Microbiol., 71, 1–20.

    Article  CAS  PubMed  Google Scholar 

  27. Dabour, N., Zihler, A., Kheadr, E., Lacroix, C., and Fliss, I. (2009) In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes, Int. J. Food Microbiol., 133, 225–233.

    Article  CAS  PubMed  Google Scholar 

  28. Charpentier, E., and Courvalin, P. (1999) Antibiotic resistance in Listeria spp., Antimicrob. Agents Chemother., 43, 2103–2108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bertsch, D., Muelli, M., Weller, M., Uruty, A., Lacroix, C., and Meile, L. (2014) Antimicrobial susceptibility and antibiotic resistance gene transfer analysis of foodborne, clinical, and environmental Listeria spp. isolates including Listeria monocytogenes, Microbiologyopen, 3, 118–127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Cintas, L. M., Casaus, P., Fernandez, M. F., and Hernandez, P. E. (1998) Comparative antimicrobial activity of enterocin L50, pediocin PA-1, nisin A and lactocin S against spoilage and foodborne pathogenic bacteria, Food Microbiol., 15, 289–298.

    Article  CAS  Google Scholar 

  31. Millette, M., Cornut, G., Dupont, C., Shareck, F., Archambault, D., and Lacroix, M. (2008) Capacity of human nisin- and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci, Appl. Environ. Microbiol., 74, 1997–2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. McClintock, M. K., Kaznessis, Y. N., and Hackel, B. J. (2016) Enterocin A mutants identified by saturation mutagenesis enhance potency towards vancomycin-resistant enterococci, Biotechnol. Bioeng., 113, 414–423.

    Article  CAS  PubMed  Google Scholar 

  33. Jimenez, J. J., Borrero, J., Gutiez, L., Arbulu, S., Herranz, C., Cintas, L. M., and Hernandez, P. E. (2014) Use of synthetic genes for cloning, production and functional expression of the bacteriocins enterocin A and bacteriocin E 50–52 by Pichia pastoris and Kluyveromyces lactis, Mol. Biotechnol., 56, 571–583.

    Article  CAS  PubMed  Google Scholar 

  34. Arbulu, S., Jimenez, J. J., Gutiez, L., Cintas, L. M., Herranz, C., and Hernandez, P. E. (2015) Cloning and expression of synthetic genes encoding the broad antimicrobial spectrum bacteriocins SRCAM 602, OR-7, E-760, and L-1077 by recombinant Pichia pastoris, Biomed. Res. Int., 2015, 767183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wachsman, M. B., Castilla, V., de Ruiz Holgado, A. P., de Torres, R. A., Sesma, F., and Coto, C. E. (2003) Enterocin CRL35 inhibits late stages of HSV-1 and HSV-2 replication in vitro, Antiviral Res., 58, 17–24.

    Article  CAS  PubMed  Google Scholar 

  36. Todorov, S. D., Wachsman, M., Tome, E., Dousset, X., Destro, M. T., Dicks, L. M. T., Franco, B. D. G. de M., Vaz-Velho, M., and Drider, D. (2010) Characterization of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium, Food Microbiol., 27, 869–879.

    Article  CAS  PubMed  Google Scholar 

  37. Lohans, C. T., and Vederas, J. C. (2012) Development of class IIa bacteriocins as therapeutic agents, Int. J. Microbiol., 2012, 386410.

    Article  CAS  PubMed  Google Scholar 

  38. Corr, S. C., Li, Y., Riedel, C. U., O’Toole, P. W., Hill, C., and Gahan, C. G. M. (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118, Proc. Natl. Acad. Sci. USA, 104, 7617–7621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Dobson, A., Cotter, P. D., Ross, R. P., and Hill, C. (2012) Bacteriocin production: a probiotic trait? Appl. Environ. Microbiol., 78, 1–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. O’Shea, E. F., Cotter, P. D., Stanton, C., Ross, R. P., and Hill, C. (2012) Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid, Int. J. Food Microbiol., 152, 189–205.

    Article  CAS  PubMed  Google Scholar 

  41. Nissen-Meyer, J., Rogne, P., Oppegard, C., Haugen, H. S., and 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.

    Article  CAS  PubMed  Google Scholar 

  42. Zouhir, A., Hammami, R., Fliss, I., and Hamida, J. B. (2010) A new structure-based classification of gram-positive bacteriocins, Protein J., 29, 432–439.

    Article  CAS  PubMed  Google Scholar 

  43. Casaus, P., Nilsen, T., Cintas, L. M., Nes, I. F., Hernandez, P. E., and Holo, H. (1997) Enterocin B, a new bacteriocin from Enterococcus faecium T136 which can act synergistically with enterocin A, Microbiology (Reading, Engl.), 143, 2287–2294.

    Article  CAS  Google Scholar 

  44. Fregeau Gallagher, N. L., Sailer, M., Niemczura, W. P., Nakashima, T. T., Stiles, M. E., and Vederas, J. C. (1997) Three-dimensional structure of leucocin A in trifluoroethanol and dodecylphosphocholine micelles: spatial location of residues critical for biological activity in type IIa bacteriocins from lactic acid bacteria, Biochemistry, 36, 15062–15072.

    Article  CAS  PubMed  Google Scholar 

  45. Wang, Y, Henz, M. E., Gallagher, N. L., Chai, S., Gibbs, A. C., Yan, L. Z., Stiles, M. E., Wishart, D. S., and Vederas, J. C. (1999) Solution structure of carnobacteriocin B2 and implications for structure-activity relationships among type IIa bacteriocins from lactic acid bacteria, Biochemistry, 38, 15438–15447.

    Article  CAS  PubMed  Google Scholar 

  46. Uteng, M., Hauge, H. H., Markwick, P. R. L., Fimland, G., Mantzilas, D., Nissen-Meyer, J., and Muhle-Goll, C. (2003) Three-dimensional structure in lipid micelles of the pediocin-like antimicrobial peptide sakacin P and a sakacin P variant that is structurally stabilized by an inserted C-terminal disulfide bridge, Biochemistry, 42, 11417–11426.

    Article  CAS  PubMed  Google Scholar 

  47. Haugen, H. S., Fimland, G., Nissen-Meyer, J., and Kristiansen, P. E. (2005) Three-dimensional structure in lipid micelles of the pediocin-like antimicrobial peptide curvacin A, Biochemistry, 44, 16149–16157.

    Article  CAS  PubMed  Google Scholar 

  48. Arbulu, S., Lohans, C. T., van Belkum, M. J., Cintas, L. M., Herranz, C., Vederas, J. C., and Hernandez, P. E. (2015) Solution structure of enterocin HF, an antilisterial bacteriocin produced by Enterococcus faecium M3K31, J. Agric. Food Chem., 63, 10689–10695.

    Article  CAS  PubMed  Google Scholar 

  49. Sit, C. S., Lohans, C. T., van Belkum, M. J., Campbell, C. D., Miskolzie, M., and Vederas, J. C. (2012) Substitution of a conserved disulfide in the type IIa bacteriocin, leucocin A, with L-leucine and L-serine residues: effects on activity and three-dimensional structure, Chembiochem, 13, 35–38.

    Article  CAS  PubMed  Google Scholar 

  50. Bedard, F., Hammami, R., Zirah, S., Rebuffat, S., Fliss, I., and Biron, E. (2018) Synthesis, antimicrobial activity and conformational analysis of the class IIa bacteriocin pediocin PA-1 and analogs thereof, Sci. Rep., 8, 9029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Fimland, G., Pirneskoski, J., Kaewsrichan, J., Jutila, A., Kristiansen, P. E., Kinnunen, P. K. J., and Nissen-Meyer, J. (2006) Mutational analysis and membrane-interactions of the beta-sheet-like N-terminal domain of the pediocin-like antimicrobial peptide sakacin P, Biochim. Biophys. Acta, 1764, 1132–1140.

    Article  CAS  PubMed  Google Scholar 

  52. Haugen, H. S., Kristiansen, P. E., Fimland, G., and Nissen-Meyer, J. (2008) Mutational analysis of the class IIa bacteriocin curvacin A and its orientation in target cell membranes, Appl. Environ. Microbiol., 74, 6766–6773.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Johnsen, L., Fimland, G., and Nissen-Meyer, J. (2005) The C-terminal domain of pediocin-like antimicrobial peptides (class IIa bacteriocins) is involved in specific recognition of the C-terminal part of cognate immunity proteins and in determining the antimicrobial spectrum, J. Biol. Chem., 280, 9243–9250.

    Article  CAS  PubMed  Google Scholar 

  54. Fimland, G., Jack, R., Jung, G., Nes, I. F., and NissenMeyer, J. (1998) The bactericidal activity of pediocin PA-1 is specifically inhibited by a 15-mer fragment that spans the bacteriocin from the center toward the C-terminus, Appl. Environ. Microbiol., 64, 5057–5060.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Yan, L. Z., Gibbs, A. C., Stiles, M. E., Wishart, D. S., and Vederas, J. C. (2000) Analogues of bacteriocins: antimicrobial specificity and interactions of leucocin A with its enantiomer, carnobacteriocin B2, and truncated derivatives, J. Med. Chem., 43, 4579–4581.

    Article  CAS  PubMed  Google Scholar 

  56. Haugen, H. S., Fimland, G., and Nissen-Meyer, J. (2011) Mutational analysis of residues in the helical region of the class IIa bacteriocin pediocin PA-1, Appl. Environ. Microbiol., 77, 1966–1972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Oppegard, C., Fimland, G., Anonsen, J. H., and Nissen-Meyer, J. (2015) The pediocin PA-1 accessory protein ensures correct disulfide bond formation in the antimicrobial peptide pediocin PA-1, Biochemistry, 54, 2967–2974.

    Article  CAS  PubMed  Google Scholar 

  58. Quadri, L. E., Yan, L. Z., Stiles, M. E., and Vederas, J. C. (1997) Effect of amino acid substitutions on the activity of carnobacteriocin B2. Overproduction of the antimicrobial peptide, its engineered variants, and its precursor in Escherichia coli, J. Biol. Chem., 272, 3384–3388.

    Article  CAS  PubMed  Google Scholar 

  59. Miller, K. W., Schamber, R., Osmanagaoglu, O., and Ray, B. (1998) Isolation and characterization of pediocin AcH chimeric protein mutants with altered bactericidal activity, Appl. Environ. Microbiol., 64, 1997–2005.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Tominaga, T., and Hatakeyama, Y. (2006) Determination of essential and variable residues in pediocin PA-1 by NNK scanning, Appl. Environ. Microbiol., 72, 1141–1147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kanatani, K., Oshimura, M., and Sano, K. (1995) Isolation and characterization of acidocin A and cloning of the bacteriocin gene from Lactobacillus acidophilus, Appl. Environ. Microbiol., 61, 1061–1067.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Stern, N. J., Svetoch, E. A., Eruslanov, B. V., Perelygin, V. V., Mitsevich, E. V., Mitsevich, I. P., Pokhilenko, V. D., Levchuk, V. P., Svetoch, O. E., and Seal, B. S. (2006) Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system, Antimicrob. Agents Chemother., 50, 3111–3116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chen, Y., Ludescher, R. D., and Montville, T. J. (1997) Electrostatic interactions, but not the YGNGV consensus motif, govern the binding of pediocin PA-1 and its fragments to phospholipid vesicles, Appl. Environ. Microbiol., 63, 4770–4777.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Kazazic, M., Nissen-Meyer, J., and Fimland, G. (2002) Mutational analysis of the role of charged residues in target-cell binding, potency and specificity of the pediocin-like bacteriocin sakacin P, Microbiology, 148, 2019–2027.

    Article  CAS  PubMed  Google Scholar 

  65. Simon, L., Fremaux, C., Cenatiempo, Y., and Berjeaud, J. M. (2002) Sakacin G, a new type of antilisterial bacteriocin, Appl. Environ. Microbiol., 68, 6416–6420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Derksen, D. J., Stymiest, J. L., and Vederas, J. C. (2006) Antimicrobial leucocin analogues with a disulfide bridge replaced by a carbocycle or by noncovalent interactions of allyl glycine residues, J. Am. Chem. Soc., 128, 14252–14253.

    Article  CAS  PubMed  Google Scholar 

  67. Fleury, Y., Dayem, M. A., Montagne, J. J., Chaboisseau, E., Le Caer, J. P., Nicolas, P., and Delfour, A. (1996) Covalent structure, synthesis, and structure-function studies of mesentericin Y 105(37), a defensive peptide from gram-positive bacteria Leuconostoc mesenteroides, J. Biol. Chem., 271, 14421–14429.

    Article  CAS  PubMed  Google Scholar 

  68. Derksen, D. J., Boudreau, M. A., and Vederas, J. C. (2008) Hydrophobic interactions as substitutes for a conserved disulfide linkage in the type IIa bacteriocins, leucocin A and pediocin PA-1, Chembiochem, 9, 1898–1901.

    Article  CAS  PubMed  Google Scholar 

  69. Mor, A., and Nicolas, P. (1994) The NH2-terminal alpha-helical domain 1–18 of dermaseptin is responsible for antimicrobial activity, J. Biol. Chem., 269, 1934–1939.

    CAS  PubMed  Google Scholar 

  70. Skerlavaj, B., Gennaro, R., Bagella, L., Merluzzi, L., Risso, A., and Zanetti, M. (1996) Biological characterization of two novel cathelicidin-derived peptides and identification of structural requirements for their antimicrobial and cell lytic activities, J. Biol. Chem., 271, 28375–28381.

    Article  CAS  PubMed  Google Scholar 

  71. Shin, S. Y., Park, E. J., Yang, S. T., Jung, H. J., Eom, S. H., Song, W. K., Kim, Y., Hahm, K. S., and Kim, J. I. (2001) Structure-activity analysis of SMAP-29, a sheep leukocytes-derived antimicrobial peptide, Biochem. Biophys. Res. Commun., 285, 1046–1051.

    Article  CAS  PubMed  Google Scholar 

  72. Xiao, Y., Dai, H., Bommineni, Y R., Soulages, J. L., Gong, Y.-X., Prakash, O., and Zhang, G. (2006) Structure-activity relationships of fowlicidin-1, a cathelicidin antimicrobial peptide in chicken, FEBS J., 273, 2581–2593.

    Article  CAS  PubMed  Google Scholar 

  73. Zhang, Y., Zhao, H., Yu, G.-Y., Liu, X.-D., Shen, J.-H., Lee, W.-H., and Zhang, Y. (2010) Structure-function relationship of king cobra cathelicidin, Peptides, 31, 1488–1493.

    Article  CAS  PubMed  Google Scholar 

  74. Fimland, G., Blingsmo, O. R., Sletten, K., Jung, G., Nes, I. F., and Nissen-Meyer, J. (1996) New biologically active hybrid bacteriocins constructed by combining regions from various pediocin-like bacteriocins: the C-terminal region is important for determining specificity, Appl. Environ. Microbiol., 62, 3313–3318.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Saavedra, L., Minahk, C., de Ruiz Holgado, A. P., and Sesma, F. (2004) Enhancement of the enterocin CRL35 activity by a synthetic peptide derived from the NH2-terminal sequence, Antimicrob. Agents Chemother., 48, 2778–2781.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Richard, C., Canon, R., Naghmouchi, K., Bertrand, D., Prevost, H., and Drider, D. (2006) Evidence on correlation between number of disulfide bridge and toxicity of class IIa bacteriocins, Food Microbiol., 23, 175–183.

    Article  CAS  PubMed  Google Scholar 

  77. Fimland, G., Johnsen, L., Axelsson, L., Brurberg, M. B., Nes, I. F., Eijsink, V. G., and Nissen-Meyer, J. (2000) A C-terminal disulfide bridge in pediocin-like bacteriocins renders bacteriocin activity less temperature dependent and is a major determinant of the antimicrobial spectrum, J. Bacteriol., 182, 2643–2648.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Kaur, K., Andrew, L. C., Wishart, D. S., and Vederas, J. C. (2004) Dynamic relationships among type IIa bacteriocins: temperature effects on antimicrobial activity and on structure of the C-terminal amphipathic alpha helix as a receptor-binding region, Biochemistry, 43, 9009–9020.

    Article  CAS  PubMed  Google Scholar 

  79. Fimland, G., Eijsink, V. G. H., and Nissen-Meyer, J. (2002) Mutational analysis of the role of tryptophan residues in an antimicrobial peptide, Biochemistry, 41, 9508–9515.

    Article  CAS  PubMed  Google Scholar 

  80. Chikindas, M. L., Garcia-Garcera, M. J., Driessen, A. J., Ledeboer, A. M., Nissen-Meyer, J., Nes, I. F., Abee, T., Konings, W. N., and Venema, G. (1993) Pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC1.0, forms hydrophilic pores in the cytoplasmic membrane of target cells, Appl. Environ. Microbiol., 59, 3577–3584.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Bruno, M. E., and Montville, T. J. (1993) Common mechanistic action of bacteriocins from lactic acid bacteria, Appl. Environ. Microbiol., 59, 3003–3010.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Minahk, C. J., Farias, M. E., Sesma, F., and Morero, R. D. (2000) Effect of enterocin CRL35 on Listeria monocytogenes cell membrane, FEMS Microbiol. Lett., 192, 79–83.

    Article  CAS  PubMed  Google Scholar 

  83. Wu, M., Maier, E., Benz, R., and Hancock, R. E. (1999) Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli, Biochemistry, 38, 7235–7242.

    Article  CAS  PubMed  Google Scholar 

  84. Minahk, C. J., Dupuy, F., and Morero, R. D. (2004) Enhancement of antibiotic activity by sub-lethal concentrations of enterocin CRL35, J. Antimicrob. Chemother., 53, 240–246.

    Article  CAS  PubMed  Google Scholar 

  85. Venema, K., Kok, J., Marugg, J. D., Toonen, M. Y., Ledeboer, A. M., Venema, G., and Chikindas, M. L. (1995) Functional analysis of the pediocin operon of Pediococcus acidilactici PAC1.0: PedB is the immunity protein and PedD is the precursor processing enzyme, Mol. Microbiol., 17, 515–522.

    Article  CAS  PubMed  Google Scholar 

  86. Chen, Y., Ludescher, R. D., and Montville, T. J. (1998) Influence of lipid composition on pediocin PA-1 binding to phospholipid vesicles, Appl. Environ. Microbiol., 64, 3530–3532.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Ramnath, M., Beukes, M., Tamura, K., and 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Dalet, K., Briand, C., Cenatiempo, Y, and Hechard, Y. (2000) The RpoN gene of Enterococcus faecalis directs sensitivity to subclass IIa bacteriocins, Curr. Microbiol., 41, 441–443.

    Article  CAS  PubMed  Google Scholar 

  89. Dalet, K., Cenatiempo, Y., Cossart, P., Hechard, Y., and European Listeria Genome Consortium (2001) A sigma(54)-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105, Microbiology, 147, 3263–3269.

    Article  CAS  PubMed  Google Scholar 

  90. Diep, D. B., Skaugen, M., Salehian, Z., Holo, H., and Nes, I. F. (2007) Common mechanisms of target cell recognition and immunity for class II bacteriocins, Proc. Natl. Acad. Sci. USA, 104, 2384–2389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kjos, M., Salehian, Z., Nes, I. F., and Diep, D. B. (2010) An extracellular loop of the mannose phosphotransferase system component IIC is responsible for specific targeting by class IIa bacteriocins, J. Bacteriol., 192, 5906–5913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Barraza, D. E., Rios Colombo, N. S., Galvan, A. E., Acuna, L., Minahk, C. J., Bellomio, A., and Chalon, M. C. (2017) New insights into enterocin CRL35: mechanism of action and immunity revealed by heterologous expression in Escherichia coli, Mol. Microbiol., 105, 922–933.

    Article  CAS  PubMed  Google Scholar 

  93. Stevens, K. A., Sheldon, B. W., Klapes, N. A., and Klaenhammer, T. R. (1991) Nisin treatment for inactivation of Salmonella species and other gram-negative bacteria, Appl. Environ. Microbiol., 57, 3613–3615.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Chalon, M. C., Acuna, L., Morero, R. D., Minahk, C. J., and Bellomio, A. (2012) Membrane-active bacteriocins to control Salmonella in foods: are they the definite hurdle? Food Res. Int., 45, 735–744.

    Article  CAS  Google Scholar 

  95. Kjos, M., Nes, I. F., and Diep, D. B. (2009) Class II one-peptide bacteriocins target a phylogenetically defined subgroup of mannose phosphotransferase systems on sensitive cells, Microbiology, 155, 2949–2961.

    Article  CAS  PubMed  Google Scholar 

  96. Opsata, M., Nes, I. F., and Holo, H. (2010) Class IIa bacteriocin resistance in Enterococcus faecalis V583: the mannose PTS operon mediates global transcriptional responses, BMC Microbiol., 10, 224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Kjos, M., Borrero, J., Opsata, M., Birri, D. J., Holo, H., Cintas, L. M., Snipen, L., Hernandez, P. E., Nes, I. F., and Diep, D. B. (2011) Target recognition, resistance, immunity and genome mining of class II bacteriocins from gram-positive bacteria, Microbiology, 157, 3256–3267.

    Article  CAS  PubMed  Google Scholar 

  98. Vadyvaloo, V., Hastings, J. W., van der Merwe, M. J., and 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Tessema, G. T., Moretro, T., Kohler, A., Axelsson, L., and 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Masias, E., Dupuy, F. G., da Silva Sanches, P. R., Farizano, J. V., Cilli, E., Bellomio, A., Saavedra, L., and Minahk, C. (2017) Impairment of the class IIa bacteriocin receptor function and membrane structural changes are associated to enterocin CRL35 high resistance in Listeria monocytogenes, Biochim. Biophys. Acta, 1861, 1770–1776.

    Article  CAS  Google Scholar 

  101. Kundig, W., Ghosh, S., and Roseman, S. (1964) Phosphate bound to histidine in a protein as an intermediate in a novel phospho-transferase system, Proc. Natl. Acad. Sci. USA, 52, 1067–1074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Postma, P. W., Lengeler, J. W., and Jacobson, G. R. (1993) Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria, Microbiol. Rev., 57, 543–594.

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Deutscher, J., Francke, C., and Postma, P. W. (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria, Microbiol. Mol. Biol. Rev., 70, 939–1031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Deutscher, J., Ake, F. M. D., Derkaoui, M., Zebre, A. C., Cao, T. N., Bouraoui, H., Kentache, T., Mokhtari, A., Milohanic, E., and Joyet, P. (2014) The bacterial phosphoenolpyruvate: carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein—protein interactions, Microbiol. Mol. Biol. Rev., 78, 231–256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Galinier, A., and Deutscher, J. (2017) Sophisticated regulation of transcriptional factors by the bacterial phosphoenolpyruvate: sugar phosphotransferase system, J. Mol. Biol., 429, 773–789.

    Article  CAS  PubMed  Google Scholar 

  106. Saier, M. H., and Paulsen, I. T. (1999) Paralogous genes encoding transport proteins in microbial genomes, Res. Microbiol., 150, 689–699.

    Article  CAS  PubMed  Google Scholar 

  107. Saier, M. H., Hvorup, R. N., and Barabote, R. D. (2005) Evolution of the bacterial phosphotransferase system: from carriers and enzymes to group translocators, Biochem. Soc. Trans., 33, 220–224.

    Article  CAS  PubMed  Google Scholar 

  108. Nguyen, T X., Yen, M.-R., Barabote, R. D., and Saier, M. H. (2006) Topological predictions for integral membrane permeases of the phosphoenolpyruvate: sugar phosphotransferase system, J. Mol. Microbiol. Biotechnol., 11, 345–360.

    Article  CAS  PubMed  Google Scholar 

  109. Cao, Y., Jin, X., Levin, E. J., Huang, H., Zong, Y, Quick, M., Weng, J., Pan, Y., Love, J., Punta, M., Rost, B., Hendrickson, W. A., Javitch, J. A., Rajashankar, K. R., and Zhou, M. (2011) Crystal structure of a phosphorylation-coupled saccharide transporter, Nature, 473, 50–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. McCoy, J. G., Ren, Z., Stanevich, V., Lee, J., Mitra, S., Levin, E. J., Poget, S., Quick, M., Im, W., and Zhou, M. (2016) The structure of a sugar transporter of the glucose EIIC superfamily provides insight into the elevator mechanism of membrane transport, Structure, 24, 956–964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Ren, Z., Lee, J., Moosa, M. M., Nian, Y., Hu, L., Xu, Z., McCoy, J. G., Ferreon, A. C. M., Im, W., and Zhou, M. (2018) Structure of an EIIC sugar transporter trapped in an inward-facing conformation, Proc. Natl. Acad. Sci. USA, 115, 5962–5967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Luo, P., Yu, X., Wang, W., Fan, S., Li, X., and Wang, J. (2015) Crystal structure of a phosphorylation-coupled vitamin C transporter, Nat. Struct. Mol. Biol., 22, 238–241.

    Article  CAS  PubMed  Google Scholar 

  113. Stock, J. B., Ninfa, A. J., and Stock, A. M. (1989) Protein phosphorylation and regulation of adaptive responses in bacteria, Microbiol. Rev., 53, 450–490.

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Fujita, Y. (2009) Carbon catabolite control of the metabolic network in Bacillus subtilis, Biosci. Biotechnol. Biochem., 73, 245–259.

    Article  CAS  PubMed  Google Scholar 

  115. Zuniga, M., Comas, I., Linaje, R., Monedero, V., Yebra, M. J., Esteban, C. D., Deutscher, J., Perez-Martinez, G., and Gonzalez-Candelas, F. (2005) Horizontal gene transfer in the molecular evolution of mannose PTS transporters, Mol. Biol. Evol., 22, 1673–1685.

    Article  CAS  PubMed  Google Scholar 

  116. Eijsink, V. G., Skeie, M., Middelhoven, P. H., Brurberg, M. B., and Nes, I. F. (1998) Comparative studies of class IIa bacteriocins of lactic acid bacteria, Appl. Environ. Microbiol., 64, 3275–3281.

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Diep, D. B., Godager, L., Brede, D., and Nes, I. F. (2006) Data mining and characterization of a novel pediocin-like bacteriocin system from the genome of Pediococcus pentosaceus ATCC 25745, Microbiology, 152, 1649–1659.

    Article  CAS  PubMed  Google Scholar 

  118. Erni, B. (2006) The mannose transporter complex: an open door for the macromolecular invasion of bacteria, J. Bacteriol., 188, 7036–7038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Fimland, G., Eijsink, V. G. H., and Nissen-Meyer, J. (2002) Comparative studies of immunity proteins of pediocin-like bacteriocins, Microbiology, 148, 3661–3670.

    Article  CAS  PubMed  Google Scholar 

  120. Fimland, G., Johnsen, L., Dalhus, B., and Nissen-Meyer, J. (2005) Pediocin-like antimicrobial peptides (class IIa bacteriocins) and their immunity proteins: biosynthesis, structure, and mode of action, J. Pept. Sci., 11, 688–696.

    Article  CAS  PubMed  Google Scholar 

  121. Johnsen, L., Fimland, G., Mantzilas, D., and Nissen-Meyer, J. (2004) Structure-function analysis of immunity proteins of pediocin-like bacteriocins: C-terminal parts of immunity proteins are involved in specific recognition of cognate bacteriocins, Appl. Environ. Microbiol., 70, 2647–2652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Sprules, T., Kawulka, K. E., and Vederas, J. C. (2004) NMR solution structure of ImB2, a protein conferring immunity to antimicrobial activity of the type IIa bacteriocin, carnobacteriocin B2, Biochemistry, 43, 11740–11749.

    Article  CAS  PubMed  Google Scholar 

  123. Johnsen, L., Dalhus, B., Leiros, I., and Nissen-Meyer, J. (2005) 1.6-angstroms crystal structure of EntA-Im. A bacterial immunity protein conferring immunity to the antimicrobial activity of the pediocin-like bacteriocin enterocin A, J. Biol. Chem., 280, 19045–19050.

    Article  CAS  PubMed  Google Scholar 

  124. Zhou, W., Wang, G., Wang, C., Ren, F., and Hao, Y. (2016) Both IIC and IID components of mannose phosphotransferase system are involved in the specific recognition between immunity protein PedB and bacteriocin—receptor complex, PLoS ONE, 11, e0164973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Nissen-Meyer, J., Havarstein, L. S., Holo, H., Sletten, K., and Nes, I. F. (1993) Association of the lactococcin A immunity factor with the cell membrane: purification and characterization of the immunity factor, J. Gen. Microbiol., 139, 1503–1509.

    Article  CAS  PubMed  Google Scholar 

  126. Quadri, L. E., Sailer, M., Terebiznik, M. R., Roy, K. L., Vederas, J. C., and Stiles, M. E. (1995) Characterization of the protein conferring immunity to the antimicrobial peptide carnobacteriocin B2 and expression of carnobacteriocins B2 and BM1, J. Bacteriol., 177, 1144–1151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Murinda, S. E., Rashid, K. A., and Roberts, R. F. (2003) In vitro assessment of the cytotoxicity of nisin, pediocin, and selected colicins on simian virus 40-transfected human colon and Vero monkey kidney cells with trypan blue staining viability assays, J. Food Prot., 66, 847–853.

    Article  CAS  PubMed  Google Scholar 

  128. Jasniewski, J., Cailliez-Grimal, C., Chevalot, I., Milliere, J.-B., and Revol-Junelles, A.-M. (2009) Interactions between two carnobacteriocins Cbn BM1 and Cbn B2 from Carnobacterium maltaromaticum CP5 on target bacteria and Caco-2 cells, Food Chem. Toxicol., 47, 893–897.

    Article  CAS  PubMed  Google Scholar 

  129. Ju, X., Chen, X., Du, L., Wu, X., Liu, F., and Yuan, J. (2015) Alanine-scanning mutational analysis of durancin GL reveals residues important for its antimicrobial activity, J. Agric. Food Chem., 63, 6402–6409.

    Article  CAS  PubMed  Google Scholar 

  130. Song, D. F., Li, X., Zhang, Y. H., Zhu, M. Y., and Gu, Q. (2014) Mutational analysis of positively charged residues in the N-terminal region of the class IIa bacteriocin pediocin PA-1, Lett. Appl. Microbiol., 58, 356–361.

    Article  CAS  PubMed  Google Scholar 

  131. Tominaga, T., and Hatakeyama, Y. (2007) Development of innovative pediocin PA-1 by DNA shuffling among class IIa bacteriocins, Appl. Environ. Microbiol., 73, 5292–5299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Acuna, L., Picariello, G., Sesma, F., Morero, R. D., and Bellomio, A. (2012) A new hybrid bacteriocin, Ent35-MccV, displays antimicrobial activity against pathogenic gram-positive and gram-negative bacteria, FEBS Open Bio, 2, 12–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Johnsen, L., Fimland, G., Eijsink, V., and Nissen-Meyer, J. (2000) Engineering increased stability in the antimicrobial peptide pediocin PA-1, Appl. Environ. Microbiol., 66, 4798–4802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Quadri, L. E., Sailer, M., Roy, K. L., Vederas, J. C., and Stiles, M. E. (1994) Chemical and genetic characterization of bacteriocins produced by Carnobacterium piscicola LV17B, J. Biol. Chem., 269, 12204–12211.

    CAS  PubMed  Google Scholar 

  135. Jasniewski, J., Cailliez-Grimal, C., Gelhaye, E., and Revol-Junelles, A.-M. (2008) Optimization of the production and purification processes of carnobacteriocins Cbn BM1 and Cbn B2 from Carnobacterium maltaromaticum CP5 by heterologous expression in Escherichia coli, J. Microbiol. Methods, 73, 41–48.

    Article  CAS  PubMed  Google Scholar 

  136. Bernbom, N., Jelle, B., Brogren, C.-H., Vogensen, F. K., Norrung, B., and Licht, T R. (2009) Pediocin PA-1 and a pediocin producing Lactobacillus plantarum strain do not change the HMA rat microbiota, Int. J. Food Microbiol., 130, 251–257.

    Article  CAS  PubMed  Google Scholar 

  137. Umu, O. C. O., Bauerl, C., Oostindjer, M., Pope, P. B., Hernandez, P. E., Perez-Martinez, G., and Diep, D. B. (2016) The potential of class II bacteriocins to modify gut microbiota to improve host health, PLoS ONE, 11, e0164036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Salvucci, E., Saavedra, L., Hebert, E. M., Haro, C., and Sesma, F. (2012) Enterocin CRL35 inhibits Listeria monocytogenes in a murine model, Foodborne Pathog. Dis., 9, 68–74.

    Article  CAS  PubMed  Google Scholar 

  139. Sosunov, V., Mischenko, V., Eruslanov, B., Svetoch, E., Shakina, Y., Stern, N., Majorov, K., Sorokoumova, G., Selishcheva, A., and Apt, A. (2007) Antimycobacterial activity of bacteriocins and their complexes with liposomes, J. Antimicrob. Chemother., 59, 919–925.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. V. Ovchinnikova.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Balandin, S.V., Sheremeteva, E.V. & Ovchinnikova, T.V. Pediocin-Like Antimicrobial Peptides of Bacteria. Biochemistry Moscow 84, 464–478 (2019). https://doi.org/10.1134/S000629791905002X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S000629791905002X

Keywords

Navigation