Abstract
Lactic acid bacteria (LAB) fight competing Gram-positive microorganisms by secreting anti-microbial peptides called bacteriocins. Peptide bacteriocins are usually divided into lantibiotics (class I) and non-lantibiotics (class II), the latter being the main topic of this review. During the past decade many of these bacteriocins have been isolated and characterized, and elements of the genetic mechanisms behind bacteriocin production have been unravelled. Bacteriocins often have a narrow inhibitory spectrum, and are normally most active towards closely related bacteria likely to occur in the same ecological niche. Lactic acid bacteria seem to compensate for these narrow inhibitory spectra by producing several bacteriocins belonging to different classes and having different inhibitory spectra. The latter may also help in counteracting the possible development of resistance mechanisms in target organisms. In many strains, bacteriocin production is controlled in a cell-density dependent manner, using a secreted peptide-pheromone for quorum-sensing. The sensing of its own growth, which is likely to be comparable to that of related species, enables the producing organism to switch on bacteriocin production at times when competition for nutrients is likely to become more severe. Although today a lot is known about LAB bacteriocins and the regulation of their production, several fundamental questions remain to be solved. These include questions regarding mechanisms of immunity and resistance, as well as the molecular basis of target-cell specificity.
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References
Abee T (1995) Pore-forming bacteriocins of Gram-positive bacteria and self-protection mechanisms of producer organisms. FEMS Microbiol. Lett. 129: 1–10.
Anderssen EL, Diep DB, Nes IF, Eijsink VGH & Nissen-Meyer J (1998) Antagonistic activity of Lactobacillus plantarum C11: two new two-peptide bacteriocins, plantaricins EF and JK, and the induction factor plantaricin A. Appl. Environ. Microbiol. 64: 2269–2272.
Axelsson L (1998) Lactic acid bacteria: classification and physiology. In: Salminen S & Von Wright A (Eds) Lactic Acid Bacteria; Microbiology and Functional Aspects, (pp 1–72). Marcel Dekker Inc., New York.
Axelsson L & Holck A (1995) The genes involved in prodcution of and immunity to sakacin A, a bacteriocin from Lactobacillus sakei Lb706. J. Bacteriol. 177: 2125–2137.
Axelsson L, Katla T, Bjørnslett M, Eijsink VGH & Holck A (1998) A system for heterologous expression of bacteriocins in Lactobacillus sakei. FEMS Microbiol. Lett. 168: 137–148.
Aymerich T, Holo, H, Håvarstein, LS, Hugas m, Garriga m & Nes IF (1996) Biochemical and genetic characterization of enterocin A from Enterococcus faecium, a new antilisterial bacteriocin in the pediocin family of bacteriocins. Appl. Environ. Microbiol. 62: 1676–1682.
Aymerich T, Artigas MG, Garriga M, Montfort JM & Hugas M (2000) Effect of sausage ingredients and additives on the production of enterocin A and B by Enterococcus faecium CTC492. Optimization of in vitro production and anti-listerial effect in dry fermented sausages. J. Appl. Microbiol. 88: 686–694.
Baba T & Schneewind O (1998) Instruments of microbial warfare: bacteriocin synthesis, toxicity and immunity. Trends Microbiol. 6: 66–71.
Bennik MHJ, Verheul A, Abee T, Naaktgeboren-Stoffels G, Gorris LGM & Smid EJ (1997) Interactions of nisin and pediocin PA-1 with closely related lactic acid bacteria that manifest over 100-fold differences in bacteriocin sensitivity. Appl. Environ. Microbiol. 63: 3628–3636.
Bennik MHJ, Vanloo B, Brasseur R, Gorris LGM & Smid EJ (1998) A novel bacteriocin with a YGNGV motif from vegetable-associated Enterococcus mundtii: full characterization and interaction with target organisms. Biochim. Biophys. Acta 1373: 47–58.
Bhugaloo-Vial P, Dousset X, Metivier A, Sorokine O, Anglade P, Boyaval P & Maron D (1996) Purification and amino acid sequences of piscicocins V1a and V1b, tow class IIa bacteriocins secreted by Carnobacterium piscicola V1 that display significantly different levels of specific inhibitory activity. Appl. Environ. Microbiol. 62: 4410–4416.
Breukink E & De Kruijff (1999) The lantibiotic nisin, a special case or not? Biochim. Biophys. Acta 1462: 223–234.
Breukink E, Wiedemann I, Van Kraaij C, Kuipers OP, 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.
Brötz H, Josten M, Wiedemann I, Schneider U, Götz F, Bierbaum G & Sahl HG (1998) Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics. Mol. Microbiol. 30: 317–327.
Bruno MEC & Montville TJ (1993) Common mechanistic action of bacteriocins from lactic acid bacteria. Appl. Environ. Microbiol. 59: 3003–3010.
Brurberg MB, Nes IF & Eijsink VGH (1997) Pheromone-induced production of antimicrobial peptides in Lactobacillus.Mol. Microbiol. 26: 347–360.
Callewaert R, Hugas M & De Vuyst L (2000) Competitiveness and bacteriocin production of Enterococci in the production of Spanish-style dry fermented saucages. Int. J. Food Microbiol. 57: 33–42.
Casaus P, Nilsen T, Cintas LM, Nes IF, Hernández PE & Holo H (1997) Enterocin B, a new bacteriocin from Enterococcus faecium T136 which can act synergistically with enterocin A. Microbiology 143: 2287–2294.
Chen Y, Ludescher RD & Montville TJ (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.
Chikindas ML, García-Garcera MJ, Driessen AJM, Ledeboer AM, Nissen-Meyer J, Nes IF, Abee T, Konings WN & Venema G (1993) Pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC1.0, forms hydrophilic pores in the cytoplasmic membrane of target cells. Appl. Envrion. Microbiol. 59: 3577–3584.
Cintas LM, Casaus P, Holo H, Hernández PE, Nes IF & Håvarstein LS (1998) Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins. J. Bacteriol. 180: 1988–1994.
Cintas LM, Casaus P, Herranz C, Håvarstein LS, Holo H, Hernández PE & Nes IF (2000) Biochemical and genetic evidence that Enterococcus faecium L50 produces Enterocins L50A and L50B, the sec-dependent Enterocin P, and a novel bacteriocin secreted without an N-terminal extension termed Enetrocin Q. J. Bacteriol. 182: 6806–6814.
Cintas LM, Casaus P, Håvarstein LS, Hernández PE & Nes IF (1997) Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum. Appl. Environ. Microbiol. 63: 4321–4330.
Claverys JP & Håvarstein LS (2002) Extracellular peptide control of competence for genetic transformation in Streptococcus pneumoniae. Front. Biosci., in press.
Dalet K, Cenatiempo Y, Cossart P, The European Listeria Genome Consortium & Héchard Y (2001) A δ54-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. Microbiology 147: 3263–3269.
Dayem MA, Fleury Y, Devilliers G, Chaboisseau E, Girard R, Nicolas P & Delfour A (1996) The putative immunity protein of the Gram-positive bacteria Leuconostoc mesenteroides is preferentially located in the cytoplasmic compartment. FEMS Microbiol. Lett. 138: 251–259.
DeSazieu A, Gardes C, Flint N, Wagner C, Kamber M, Mitcehll TJ, Kekck W, Amrein KE & Lange R (2000) Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide. J Bacteriol. 182: 4696–4703.
Diep DB, Axelsson L, Grefsli C & Nes IF (2000) The synthesis of the bacteriocin sakacin A is a temperature-sensitive process regulated by a pheromone peptide through a three-component regulatory system. Microbiology 146: 2155–2160.
Diep DB, Håvarstein LS & Nes IF (1995) A bacteriocin-like peptide induces bacteriocin synthesis in Lactobacillus plantarum C11. Mol. Microbiol. 18: 631–639.
Diep DB, Håvarstein LS & Nes IF (1996) Characterization of the locus responsible for the bacteriocin production in Lactobacillus plantarum C11. J. Bacteriol. 178: 4472–4483.
Diep DB, Johnsborg O, Risøen PA & Nes IF (2001) Evidence for dual functionality of the operon plnABCD in the regulation of bacteriocin production in Lactobacillus plantarum. Mol. Microbiol. 41: 633–644.
Donvito B, Etienne J, Denoroy L, Greenland T, Benito Y & Vandenesch F (1997) Synergistic hemolytic activity of Staphylococcus lugdunensis is mediated by three peptides encoded by a non-agr genetic locus. Infect. Immun. 65: 95–100.
Driessen AJM, Van den Hooven HW, Kuiper W, Van den Kemp M, Sahl HG, Konings RNH & Konings WN (1995) Mechanistic studies of lantibiotic-induced permeabilization of phospholipid vesicles. Biochemistry 34: 1606–1614.
Duffes F, Leroi F, Dousset X & Boyaval P (2000) use of bacteriocin producing Carnobacterium piscicola strain, isolated from fish, to control Listeria monocytogenes development in vacuum-packed cold-smoked salmon stored at 4 degrees C. Sciences des Aliments 20: 153–158.
Dykes GA (1995) Bacteriocins: ecological and evolutionary significance. Trends Ecol. Evol. 10: 186–189.
Ehrmann MA, Remiger A, Eijsink VGH & Vogel RF (2000) A gene cluster encoding planatricin 1.25 ß and other bacteriocin-like peptides in Lactobacillus plantarum TMW1.25. Bioch. Biophys. Acta 1490: 355–361.
Eijsink VGH, Brurberg MB, Middelhoven PJ & Nes IF (1996) Induction of bacteriocin prodcution in Lactobacillus sakei by a secreted peptide. J. Bacteriol. 178: 2232–2237.
Eijsink VGH, Skeie M, Middelhoven PH, Brurberg MB & Nes IF (1998) Comparative studies of class IIa bacteriocins of lactic acid bacteria. Appl. Environ. Microbiol. 64: 3275–3281.
Ennahar S, Sashihara T, Sonomoto K & Ishizaki A (2000) Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24: 85–106.
Ennahar S, Sonomoto K & Ishizaki A (1999) Class IIa bacteriocins from lactic acid bacteria: antibacterial activity and food preservation. J. Biosci. Bioeng. 87: 705–716.
Fimland G, Blingsmo OR, Sletten K, Jung G, Nes IF & 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.
Fimland G, Jack R, Jung G, Nes IF & Nissen-Meyer J (1998) The bactericidal activity of pediocin PA-1 is specifically inhibited by a 15-mer fragment that spans the bacteriocin from the center towards the C-terminus. Appl. Environ. Microbiol. 64: 5057–5060.
Fimland G, Johnsen L, Axelsson L, Brurberg MB, Nes IF, Eijsink VGH & 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.
Fimland G, Eijsink VGH & Nissen-Meyer J (2002) Mutational analysis of the role of tryptophan residues in an antimicrobial peptide. Biochemistry, in press.
Fleury Y, Dayem MA, Montagne JJ, Chaboisseau E, Le Caer JP, Nicolas P & Delfour A (1996) Covalent structure, synthesis and structure-function studies of mesentericin Y 10537, a defensive peptide from Gram-positive bacteria Leuconostoc mesenteroides. J. Biol. Chem. 271: 14421–14429.
Franz CMAP, Worobo RW, Quadri LEN, Schillinger U, Holzapfel WH, Vederas JC & Stiles ME (1999) Atypical genetic locus associated with constitutive production of enterocin B by Enterococcus faecium BFE900. Appl. Environ. Microbiol. 65: 2170–2178.
Franz CMAP, Van Belkum MJ, Worobo RW, Vederas JC & Stiles ME (2000) Characterization of the genetic locus responsible for production and immunity of carnobacteriocin A: the immunity gene confers cross-protection to enterocin B. Microbiology 146: 621–631.
Fremaux C, Héchard Y & Cenatiempo Y (1995) Mesentericin Y105 gene clusters in Leuconostoc mesenteroides Y105. Microbiology 141: 1637–1645.
Fregeau Gallagher NL, Sailer M, Niemczura WP, Nakashima TT, Stiles ME & Vederas JC (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.
Gonzalez B, Glaasker E, Kunji ERS, Driessen AJM, Suarez JE & Konings WN (1996) Bactericidal mode of action of plantaricin C. Appl. Environ. Microbiol. 62: 2701–2709.
Hastings JW, Sailer M, Johnson K, Roy KL, Vederas JC & Stiles ME (1991) Characterization of leucocin A-UAL 187 and cloning of the bacteriocin gene form Leuconostoc gelidum. J. Bacteriol. 173: 7491–7500.
Hauge HH, Nissen-Meyer J, Nes IF & Eijsink VGH (1998a) Amphiphilic α-helices are important structural motifs in the α and β peptides that constitute the bacteriocin lactococcin G. Enhancement of helix formation upon α-β-interaction. Eur. J. Biochem. 251: 565–572.
Hauge HH, Mantzilas D, Moll GN, Konings WN, Driessen AJM, Eijsink VGH & Nissen-Meyer J (1998b) Plantaricin A is an amphiphilic α-helical bacteriocin-like pheromone which exerts antimicrobial and pheromone activities through different mechanisms. Biochemistry 37: 16026–16032.
Hauge HH, Mantzilas D, Eijsink VGH & Nissen-Meyer J (1999) Membrane-mimicking entities induce structuring of the two-component bacteriocins plantaricin E/F and plantaricin J/K. J. Bacteriol. 181: 740–747.
Håvarstein LS, Diep DB & Nes IF (1995) A family of ABC-transporters carry out proteolytic processing of their substrates concomitant with export. Mol. Microbiol. 16: 229–240.
Håvarstein LS, Holo H & Nes H (1994) The leader peptide of colicin V shares consensus sequences with leader peptides that are common among peptide bacteriocins produced by Gram-positive bacteria. Microbiology 140: 2383–2389.
Håvarstein LS & Morrison DA (1999) Quorum-sensing and peptide pheromones in streptococcal competence for genetic transformation. In: Dunny GM & Winans SC (Eds) Cell-Cell Signaling in Bacteria (pp 9–26). American Society for Microbiology, Washington D.C.
Héchard Y, Pelletier C, Cenatiempo, Y & Frere, J (2001) Analysis of σ54-dependent genes in Enterococcus faecalis: a mannose PTS permease (EII Man ) is involved in sensitivitiy to a bacteriocin, mesentericin Y105. Microbiology 147: 1575–1580.
Henderson JT, Chopko AL & Van Wassenaar PD (1992) Purification and primary structure of pediocin PA-1 produced by Pediococcus acidilactici PAC-1.0. Arch. Biochem. Biophys. 295: 5–12.
Herranz C, Chen Y, Chung HJ, Cintas LM, Hernandez PE, Montville TJ & Chikindas MJ (2001a) Enterocin P selectively dissipates the membrane potential of Enterococcus faecium T136. Appl. Environ. Microbiol. 67: 1689–1692.
Herranz C, Cintas LM, Hernandez PE, Moll GN & Driessen AJM (2001b) Enterocin P causes potassium ion efflux from Enterococcus faecium T136 cells. Antimicr. Agents Chemoth. 45: 901–904.
Holo H & Nes IF (2000) Class II antimicrobial peptides from lactic acid bacteria. Biopolymers 55: 50–61.
Holo H, Jeknic Z, Daeschel M, Stevanovic S & Nes IF (2001) Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology 147: 643–651.
Hühne K, Holck A, Axelsson L & Kroeckel L (1996) Analysis of the sakacin P gene cluster from Lactobacillus sakei Lb674 and its expression in sakacin-negative Lb. sakei strains. Microbiology 142: 1437–1448.
Jack RW, Wan J, Gordon J, Harmark K, Davidson BE, Hillier AJ, Wettenhall REH, Hickey MW & Coventry MJ (1996) Characterization of the chemical and antimicrobial properties of piscicolin 126, a bacteriocin produced by Carnobacterium piscicola JG126. Appl. Environ. Microbiol. 62: 2897–2903.
Johnsen L, Fimland G, Eijsink VGH & Nissen-Meyer J (2000) Engineering increased stability in the antimicrobial peptide pediocin PA-1. Appl. Environ. Microbiol. 66: 4798–4802.
Kaiser AL & Montville TJ (1996) Purification of the bacteriocin bavaricin MN and characterization of its mode of action against Listeria monocytogenes Scott A cells and lipid vesicles. Appl. Envrion. Microbiol. 62: 4529–4535.
Kalmokoff ML, Banerjee SK, Cyr T, Hefford MA & Gleeson T (2001) Identification of a new plasmid-encoded sec-dependent bacteriocin produced by Listeria innocua 743. Appl. Environ. Microbiol. 67: 4041–4047.
Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12: 39–86.
Kleerebezem M, De Vos WM & Kuipers OP (1999) The lantibiotics nisin and subtilin act as extracellular regulators of their own synthesis. In: Dunny GM & Winans SC (Eds) Cell-Cell Signaling in Bacteria (pp 159–174). American Society for Microbiology, Washington D.C.
Kleerebezem M & Quadri LEN (2001) Peptide pheromone-dependent regulation of antimicrobial peptide production in Gram-positive bacteria: a case of multicellular behaviour. Peptides 22: 1579–1596.
Kleerebezem M, Kuipers OP, De Vos WM, Stiles ME & Quadri LEN (2001) A two-component signal-transduction cascade in Carnobacterium piscicola LV17B: two signalling peptides and one sensor-transmitter. Peptides 22: 1597–1601.
Kuipers OP, Beerthuyzen Mm, De Ruyter PGGA, Luesink EJ & De Vos WM (1995) Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J. Biol. Chem. 270: 27299–27304.
Lacks SA & Greenberg B (2001) Constitutive competence for genetic transformation in Streptococcus pneumoniae caused by mutation of a transmembrane histidine kinase. Mol. Microbiol. 42: 1035–1045.
Larsen AG, Vogensen FK & Josephsen J (1993) Antimicrobial activity of lactic acid bacteria isolated from sour doughs; purification and characterization of bavaricin A, a bacteriocin produced by Lactobacillus bavaricus MI401. J. Appl. Bacteriol. 75: 113–122.
Leal MV, Baras M, Ruiz-Barba JL, Floriano B & Jimenez-Diaz R (1998) Bacteriocin production and competitiveness of Lactobacillus plantarum LPCO10 in olive juice broth, a culture medium obtained from olives. Int. J. Food Microbiol. 43: 129–134.
LeMarrec C, Hyronimus B, Bressollier P, Verneuil B & Urdaci MC (2000) Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I4. Appl. Environ. Microbiol. 66: 5213–4220.
Lian LY, Chan WC, Morley SD, Roberts GCK, Bycroft BW & Jackson D (1992) Solution structures of nisin A and its 2 major degradation products determined by NMR. Biochem. J. 283: 413–420.
Marciset O, Jeronimus-Stratingh MC, Mollet B & Poolman B (1997) Thermophilin 13, a nontypical antilisterial poration complex bacteriocin, that functions without a receptor. J. Biol. Chem. 272: 14277–14284.
Martin B, Prudhomme M, Alloing G, Granadel C & Claverys JP (2000) Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol. Microbiol. 38: 867–878.
Marugg JD, Gonzalez CF, Kunka BS, Ledeboer AM, Pucci MJ, Toonen MY, Walker SA, Zoetmulder LCM & Vandenbergh, PA (1992) Cloning, expression, and nucleotide sequence of genes involved in production of pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC1.0. Appl. Environ. Microbiol. 58: 2360–2367.
McAuliffe O, Ross RP & Hill C (2001) Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiol. Rev. 25: 285–308.
McCafferty DG, Cudic P, Yu MK, Behenna DC & Kruger R (1999) Synergy and duality in peptide antibiotic mechanisms. Curr. Opin. Chem. Biol. 3: 672–680.
Metivier A, Pilet MF, Dousset X, Sorokine O, Anglade P. Zagorec M, Piard JC, Marion D, Cenatiempo Y & Frmaux C (1998) Divercin V41, a new bacteriocin with two disulphide bonds produced by Carnobacterium divergens V41: primary structure and genomic organization. Microbiology 144: 2837–2844.
Michiels J, Dirix G, Vanderleyden J & Xi C (2001) Processing and export of peptide pheromones and bacteriocins in Gram-negative bacteria. Trends Microbiol. 9: 164–168.
Miller K, Schamber R, Osmanagaoglu O & Ray B (1998) Isolation and characterization of pediocin AcH chimeric protein mutants with altered bactericidal activity. Appl. Environ. Microbiol. 64: 1997–2005.
Ming XT, Weber GH, Ayres JW & Sandine WE (1997) Bacteriocins applied to food packaging materials to inhibit Listeria monocytogenes on meats. J. Food Sci. 62: 413–415.
Moll GN, Ubbink-Kok T, Hauge HH, Nissen-Meyer J, Nes IF, Konings WN & Driessen AJM (1996) Lactococcin G is a potassium ion-conducting two-component bacteriocin. J. Bacteriol. 178: 600–650.
Moll GN, Van den Akker E, Hauge HH, Nissen-Meyer J, Nes IF, Konings WN & Driessen AJM (1999a) Complementary and overlapping selectivity of the two-peptide bacteriocins plantaricin EF and JK. J. Bacteriol. 181: 4848–4852.
Moll GN, Konings WN & Driessen AJM (1999b) Bacteriocins: mechanism of membrane insertion and pore formation. Antonie van Leeuwenhoek 76: 185–189.
Montville TJ & Chen Y (1998) Mechanistic action of pediocin and nisin: recent progress and unresolved questions. Appl. Microbiol. Biotechnol. 50: 511–519.
Møretrø T (2000) Optimization of production of the bacteriocin sakacin P by Lactobacillus sakei; cultural conditions and genetics. Academic Thesis, Agricultural University of Norway.
Motlagh AM, Bhunia AK, Szostek F, Hansen TR, Johnson MC & Ray B (1992) Nucleotide and amino-acid sequence of pap-gene (pediocin AcH production in Pediococcus acidolactici H. Lett. Appl. Microbiol. 15: 45–48.
Navaratna MA, Sahl HG & Tagg JR (1998) Two-component anti-Staphylococcus aureus lantibiotic activity produced by Staphylococcus aureus C55. Appl. Environ. Microbiol. 64: 4803–4808.
Nes IF, Diep DB, Håvarstein LS, Brurberg MB, Eijsink VGH & Holo H (1996) Biosynthesis of bacteriocins in lactic acid bacteria. Antonie van Leeuwenhoek 70: 113–128.
Nes IF & Eijsink VGH (1999) Regulation of group II peptide bacteriocin synthesis by quorum-sensing mechanisms. In: Dunny GM & Winans SC (Eds) Cell-Cell Signaling in Bacteria (pp 175–192). American Society for Microbiology, Washington D.C.
Nes IF & Holo H (2000) Class II antimicrobial peptides from lactic acid bacteria. Biopolymers 55: 50–61.
Nieto Lozano JC, Nissen Meyer J, Sletten K, Pelaz C & Nes IF (1992) Purification and amino acid sequence of a bacteriocin produced by Pediococcus acidilactici. J. Gen. Microbiol. 138: 1985–1990.
Nilsen T, Nes IF & Holo H (1998) An exported inducer peptide regulates bacteriocin production in Enterococcus faecium CTC492. J. Bacteriol. 180: 1848–1854.
Nissen-Meyer J, Håvarstein LS, Holo G, Sletten K & Nes IF (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.
Nissen-Meyer J, Holo H, Håvarstein LS, Sletten K & Nes IF (1992) A novel lactococcal bacteriocin whose activity depends on the complementary action of two peptides. J. Bacteriol. 174: 5686–5692.
Ojcius DM & Young JDE (1991) Cytolytic pore-forming proteins and peptides: is there a common structural motif? Trends Biochem. Sci. 16: 225–229.
Oumer A, Gaya P, Fernandez-Garcia E, Mariaca R, Garde S, Medina M & Nunez M (2001) Proteolysis and formation of volatile compounds in cheese manufactured with a bacteriocin-producing adjunct culture. J. Dairy Res. 68: 117–129.
Papathanasopoulos MA, Dykes GA, Revol-Junelles A-M, Delfour A, Von Holy A & Hastings JW (1998) Sequence and structural relationships of Leucocins A-, B-and C-TA33a from Leuconostioc mesenteroides TA33a. Microbiology 144: 1343–1348.
Pei J & Grishin NV (2001) Type II CAAX prenyl endopeptidases belong to a novel superfamily of putative membrane-bound metalloproteases. Trends Biochem. Sci. 26: 275–277.
Quadri LEN, Sailer M, Roy KL, Vederas JC & Stiles ME (1994) Chemical and genetic characterization of bacteriocins produced by Carnobacterium piscicola LV17B. J. Biol. Chem. 269: 12204–12211.
Quadri LEN, Sailer M, Terebiznik MR, Roy KL, Vederas JC & Stiles ME (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.
Quadri LEN, Yan LZ, Stiles ME & Vederas JC (1997a) Effect of amino acid substitutions on the activity of carnobacteriocins B2. J. Biol. Chem. 272: 3384–3388.
Quadri LEN, Kleerebezem M, Kuipers OP, De Vos WM, Roy KL, Vederas JC & Stiles ME (1997b) Characterization of a locus from Carnobacterium piscicola LV17B involved in bacteriocin production and immunity: evidence fro global inducer-mediated transcriptional control. J. Bacteriol. 179: 6163–6171.
Ramnath M, Beukes M, Tamura K & Hastings JW (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.
Reichmann P & Hakenbeck R (2000) Allelic variation in a peptide-inducible two-component system of Streptococcus pneumoniae. FEMS Microbiol. Lett. 190: 231–236.
Riley MA & Gordon DM (1999) The ecological role of bacteriocins in bacterial competition. Trends Microbiol. 7: 129–133.
Risøen PA, Håvarstein LS, Diep BD & Nes IF (1998) Identification of the DNA-binding sites fro two response regulators involved in control of bacteriocin synthesis in Lactobacillus plantarum C11. Mol. Gen. Genet. 259: 224–232.
Risøen PA, Brurberg MB, Eijsink VGH & Nes IF (2000) Functional analysis of promoters involved in quorum sensing-based regulation of bacteriocin production in Lactobacillus. Mol. Microbiol. 37: 619–628.
Risøen PA, Johnsborg O, Diep DB, Hamoen L, Venema G & Nes IF (2001) Regulation of bacteriocin production in Lactobacillus plantarum depends on a conserved promoter arrangement with consensus binding sequence. Mol. Genet. Genomics 265: 198–206.
Ruiz-Barba JL, Cathart DP, Warner PJ & Jimenez-Diaz R (1994) Use of Lactobacillus plantarum LPCO10, a bacteriocin producer, as a starter culture in Spanish-style green oliv fermentations. Appl. Environ. Microbiol. 60: 2059–2064.
Ryan MP, Rea MC, Hill C & Ross RP (1996) An application in cheddar cheese manufacture for a strain of Lactococcus lactis producing a novel broad-spectrum bacteriocin, lacticin 3147. Appl. Environ. Microbiol. 64: 612–619.
Ryan MP, Jack RW, Josten M, Sahl HG, Ross RP & Hill C (1999) Extensive post-translational modification, including serine to D-alanine conversion, in the two-component lantibiotic lacticin 3147. J. Biol. Chem. 274: 37544–37550.
Ryan MP, Ross RP & Hill C (2001) Strategy for manipulation of cheese flora using combinations of lacticin 3147-producing and resistant cultures. Appl. Environ. Microbiol. 67: 2699–2704.
Sahl HG & Bierbaum G (1998) Lantibiotics: biosynthesis and biological activities of uniquely modified peptides from Gram-positive bacteria. Ann. Rev. Microbiol. 52: 41–79.
Saucier L, Poon A & Stiles ME (1995) Induction of bacteriocin production in Carnobacterium piscicola LV17. J. Appl. Microbiol. 78: 684–690.
Schnell N, Entian KD, Schneider U, Götz F, Zahner H, Kellner R & Jung G (1988) Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide rings. Nature 333: 276–278.
Tichaczek PS, Nissen-Meyer J, Nes IF, Vogel RF & Hammes WP (1992) Characterization of the bacteriocins curvacin A from Lactobacillus curvatus LTH1174 and sakacin P from L. sakei LTH673. System. Appl. Microbiol. 15: 460–468.
Tomita H, Fujimoto S, Tanimoto K & Ike Y (1996) Cloning and genetic organization of the bacteriocin 31 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pYI17. J. Bacteriol. 178: 3583–3593.
Van Belkum MJ, Kok J, Venema G, Holo H, Nes IF, Konings WN & Abee T (1991) The bacteriocin lactococcin A specifically increases permeability of lactococcal cytoplasmic membranes in a voltage-dependent, protein-mediated manner. J. Bacteriol. 173: 7934–7941.
Van Belkum MJ, Worobo RW & Stiles ME (1997) Double-glycine-type leader peptides direct secretion of bacteriocins by ABC transporters: colicin V secretion in Lactococcus lactis. Mol. Microbiol. 23: 1293–1301.
Van den Hooven HW, Doeland CCM, Van de Kamp M, Konings RNH, Hilbers CW & Van de Ven FJM (1996) Three-dimensional structure of the lantibiotic nisin in the presence of membrane-mimetic micelles of dodecylphosphocholine and sodium dodecylphosphate. Eur. J. Biochem. 235: 382–393.
Van den Hooven HW, Fogolari F, Rollema HS, Konings RNH, Hilbers CW & Van de Ven FJM (1993) NMR and circular dichroism studies of the lantibiotic nisin in non-aqueous environments. FEBS Lett. 319: 189–194.
Van de Ven FJM, Van den Hooven HW, Konings RNH & Hilbers CW (1991) NMR-studies of lantibiotics - The structure of nisin in aqueous solution. Eur. J. Biochem. 202: 1181–1188.
Venema K, Venema G & Kok J (1995) Lactococcal bacteriocins: mode of action and immunity. Trends Microbiol. 8: 299–304.
Vogel RF, Pohle BS, Tichczek PS & Hammes WP (1993) The competitive advantage of Lactobacillus curvatus LTH1174 in sausage fermentations is caused by formation of curvacin A. Syst. Appl. Microbiol. 16: 457–462.
Wang Y, Henz ME, Fregeau Gallagher N, Chai S, Gibbs AC, Yan LZ, Stiles ME, Wishart DS & Vederas JC (1999) Solution structure of carnobacteriocin B2 and implications for structure-activity relationships among type IIa bacteriocins from lactic acid bacteria. Biochemistry 38: 15438–15447.
Weinbrenner DR, Barefoot SF & Grinstead DA (1997) Inhibition of yoghurt starter cultures by jenseniin G, a Proprionibacterium bacteriocin. J. Dairy Sci. 80: 1246–1253.
West AH & Stock AM (2001) Histidine kinases and response regulator proteins in two-component signalling systems. Trends Biochem. Sci. 26: 369–376.
Yan LZ, Gibbs AC, Stiles ME, Wishart DS & Vederas JC (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.
Yildirim Z, Winters DK & Johnson Mg (1999) Identification, amino acid sequence and mode of action of bifidocin B produced by Bifidobacterium bifidum NCFB 1454. J. Appl. Microbiol. 86: 45–54.
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Eijsink, V.G., Axelsson, L., Diep, D.B. et al. Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie Van Leeuwenhoek 81, 639–654 (2002). https://doi.org/10.1023/A:1020582211262
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DOI: https://doi.org/10.1023/A:1020582211262