Regulation of Class II Bacteriocin Production by Cell-Cell Signaling

  • Quadri, Luis E.N. (Weill Medical College of Cornell University, Department of Microbiology and Immunology)
  • Published : 2003.09.01

Abstract

Production of ribosomally synthesized antimicrobial peptides usually referred to as bacteriocins is an inducible trait in several gram positive bacteria, particularly in those belonging to the group of lactic acid bacteria. In many of these organisms, production of bacteriocins is inducible and induction requires secretion and extracellular accumulation of peptides that act as chemical messengers and trigger bacteriocin production. These inducer peptides are often referred to as autoinducers and are believed to permit a quorum sensing-based regulation of bacteriocin production. Notably, the peptides acting as autoinducers are dedicated peptides with or without antimicrobial activity or the bacteriocins themselves. The autoinducer-dependent induction of bacteriocin production requires histidine protein kinases and response regulator proteins of two-component signal transduction systems. The current working model for the regulation of class II bacteriocin production in lactic acid bacteria and the most relevant direct and indirect pieces of evidence supporting the model are discussed in this minireview.

Keywords

References

  1. J.Bacteriol v.177 The genes involved in production of and immunity to sakacin A, a bacteriocin from Lactobacillus sake Lb706 Axelsson,L.;A.Holck https://doi.org/10.1128/jb.177.8.2125-2137.1995
  2. Appl. Environ. Microbiol. v.59 Cloning and nucleotide sequence of a gene from Lactobacillus sake Lb706 necessary for sakacin A production and immunity Axelsson,L.;A.Holck;S.E.Birkeland;T.Aukrust;H.Blom
  3. Curr. Opin. Neurobiol. v.1 G proteins and G-protein-coupled receptors:structure, function and interactions Bockaert,J. https://doi.org/10.1016/0959-4388(91)90008-U
  4. Biochem.J. v.370 Photolabelling the rat urotensin Ⅱ/GPR14 receptor identifies a ligand-blinding site in the fourth transmembrane domain Boukard,A.A.;S.S.Sauve;G.Guillemette;E.Escher;R.Leduc https://doi.org/10.1042/BJ20021566
  5. Mol. Microbiol. v.26 Pheromone-induced production of antimicrobial peptides in Lactobacillus Brurberg,M.B.;I.F.Nes;V.G.Eijsink https://doi.org/10.1046/j.1365-2958.1997.5821951.x
  6. Mol. Microbiol. v.18 A bacteriocin-like peptide induces bacteriocin synthesis in Lactobacillus plantarum C11 Diep,D.B.;L.S.Havarstein;I.F.Nes https://doi.org/10.1111/j.1365-2958.1995.mmi_18040631.x
  7. J. Bacteriol v.178 Characterization of the locus responsible for the bacteriocin production in Lactobacillus plantarum C11 Diep,D.B.;L.S.Havarstein;I.F.Nes https://doi.org/10.1128/jb.178.15.4472-4483.1996
  8. Appl. Environ. Microbiol. v.60 The gene encoding plantricin A, a bacteriocin from Lactobacillus plantarum C11, is located on the same transcription unit as an agr-like regulatory system Diep,D.B.;L.S.Havarstein;J.Nissen-Meyer;I.F.Nes
  9. Microbiology v.146 The sysnthesis of the bactiriocin sakacin A is a temperature-senstive process regulated by a pheromone peptide through a three-component regulatory system Diep,D.B.;L.Axelsson;C.Grefsli;I.F.Nes https://doi.org/10.1099/00221287-146-9-2155
  10. Mol. Microbiol. v.41 Evidence for dual functionality of the operon plnABCD in the regulation of bacteriocin production in Lactobacillus plantarum Diep,D.B.;O.Johnsborg;P.A.Risoen;I.F.Nes https://doi.org/10.1046/j.1365-2958.2001.02533.x
  11. Mol. Microbiol. v.47 Inducible bacteriocin production in Lactobacillus is regulated by differential expression of the pln operons and by two antagonizing response regulators, the activity of which is enhanced upon phosphorylation Diep,D.B.;R.Myhre;O.Johnsborg;A.Aakra;I.F.Nes https://doi.org/10.1046/j.1365-2958.2003.03310.x
  12. Microbiology v.142 Molecular analysis of the regulation of nisin immunity Dodd,H.M.;N.Horn;W.C.Chan;C.J.Giffard;B.W.Bycroft;G.C.Robert;M.J.Gasson https://doi.org/10.1099/00221287-142-9-2385
  13. Cell-cell signaling in bacteria, (1st ed.) Dunny,G.M.(ed.);S.C.Winans(ed.)
  14. J. Bacteriol v.178 Induction of bacteriocin production in Lactobacillus sake by a secreted peptide Eijsink,V.G.;M.B.Brurberg;P.H.Middelhoven;I.F.Nes https://doi.org/10.1128/jb.178.8.2232-2237.1996
  15. FEMS Microbiol. Rev. v.24 Class IIa bacteriocins: biosynthesis, structure and activity Ennahar,S.;T.Sashihara;K.Sonomoto;A.Ishizaki https://doi.org/10.1111/j.1574-6976.2000.tb00534.x
  16. FEMS Microbiol. Lett. v.186 Simple method to identify bacteriocin induction peptides and to autoinduce bacteriocin production at low cell density Franz,C.M.;M.E.Stiles;M.J. van Belkum https://doi.org/10.1111/j.1574-6968.2000.tb09101.x
  17. Microbiology v.146 Chracterization of the genetic locus responsible for production and immunity of carmobacteriocin A: the immunity gene confers cross-protection to enterocin B. Franz,C.M.;M.J. van Belkum;R.W.Worobo;J.C.Vederas;M.E.Stiles https://doi.org/10.1099/00221287-146-3-621
  18. Annu. Rev. Genet v.35 Regulation of gene expression by cell-to-cell communication: acy1-homoserine lactone quorum sensing Fuqua,C.;M.R.Parsek;E.P.Greenberg https://doi.org/10.1146/annurev.genet.35.102401.090913
  19. Biopolymers v.55 Posttranslationally modified bacteriocins-the lantibiotics Guder,A.;I.Wiedemann;H.G.Sahl https://doi.org/10.1002/1097-0282(2000)55:1<62::AID-BIP60>3.0.CO;2-Y
  20. Biochemistry v.37 Plantaricin A is an amphiphilic alpha-helical bacteriocin-like pheromone which exerts antimicrobial and pheromone activities through different mechanisms Hauge,H.H.;D.Mantzilas;G.N.Moll;W.N.Konings;A.J.Driessen;V.G.Eijsink;J.Nissen-Meyer https://doi.org/10.1021/bi981532j
  21. Mol. Microbiol. v.16 A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export H$\aa$varstein,L.S.;D.B.Diep;I.F.Nes https://doi.org/10.1111/j.1365-2958.1995.tb02295.x
  22. Mol. Microbiol. v.21 Identification of the streptococcal competence-pherimone receptor H$\aa$varstein,L.S.;P.Gaustad;I.F.Nes;D.A.Morrison https://doi.org/10.1046/j.1365-2958.1996.521416.x
  23. Biochemistry v.41 Identification of a contact region between the tridecapeptide alpha-factor mating pheromone of Saccharomyces cerevisiae and its G protein-coupled receptor by photoaffinity labeling Henry,L.K.;S.Khare;C.Son;V.V.Babu;F.Naider;J.M.Becker https://doi.org/10.1021/bi015863z
  24. Microbiology v.142 Analysis of the sakacin P gene cluster from Lactobacillus sake Lb674 and its expression in sakacin-negative Lb. sake stains Huhne,K.;L.Axelsson;A.Holck;L.Krockel https://doi.org/10.1099/13500872-142-6-1437
  25. Curr.Opin.Chem.Biol. v.4 Lantibiotics and microcins: polypeptides with unusual chemical diversity Jack,R.W.;G.Jung https://doi.org/10.1016/S1367-5931(00)00094-6
  26. FEMS Microbiol. Rev. v.12 Genetics of bacteriocins produced by lactic acid bacteria Klaenhammer,T.R.
  27. Peptides v.22 Peptide pheromone-dependent regulation of antimicrobial peptide prodection in gram positive bacteria: a case of multicellular bahavior Kleerebezem,M.;L.E.Quadri https://doi.org/10.1016/S0196-9781(01)00493-4
  28. Mol. Microbiol. v.24 Quorum sensing by peptide pheromones and two-component signal-transduction systems in gram positive bacteria Kleerebezem,M.;L.E.Quadri;O.P.Kuipers;W.M. de Vos https://doi.org/10.1046/j.1365-2958.1997.4251782.x
  29. Peptides v.22 A two-component signal-transduction cascade in Carnobacterium piscicola LV17B: two signaling peptides and one sensor-transmitter Kleerebezem,M.;O.P.Kuipers;W.M. de Vos;M.E.Stiles;L.E.Quadri https://doi.org/10.1016/S0196-9781(01)00494-6
  30. Eur. J. Biochem. v.216 Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis.Requirement of expression of the nisA and nisI genes for development of immunity Kuipers,O.P.;M.M.Beerthuyzen;R.J.Siezen;W.M. de Vos. https://doi.org/10.1111/j.1432-1033.1993.tb18143.x
  31. J. Biol. Chem. v.270 Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction Kuipers,O.P.;M.M.Beerthuyzen;P.G. de Ruyter;E.J.Luesink;W.M. de Vos. https://doi.org/10.1074/jbc.270.45.27299
  32. Mol. Microbiol. v.12 Identification and molecular analysis of a locus that regulates extracellular toxin production in Clostridium perfringns Lyristics,M.;A.E.Bryant;J.Sloan;M.M.Award;I.T.Nisbet;D.L.Stevens;J.I.Rood https://doi.org/10.1111/j.1365-2958.1994.tb01063.x
  33. subtilis. Cell v.77 Biochemical and genetic characterization of a competence pheromone from B Magnuson,R.;J.Solomon;A.D.Grossman https://doi.org/10.1016/0092-8674(94)90313-1
  34. FEMS Microbiol. Rev. v.25 Lantibiotics: structure, biosynthesis and mode of action McAuliffe,O.;R.P.Ross;C.Hill https://doi.org/10.1111/j.1574-6976.2001.tb00579.x
  35. Annu. Rev. Microbiol. v.55 Quorum sensing in bacteria Miller,M.B.;B.L.Bassler https://doi.org/10.1146/annurev.micro.55.1.165
  36. Biopolymers v.55 Class Ⅱ antimicrobial peptides from lactic acid bacteria Nes,I.F.;H.Holo https://doi.org/10.1002/1097-0282(2000)55:1<50::AID-BIP50>3.0.CO;2-3
  37. Antonie Van Leeuwenhoek v.70 Biosynthesis of bacteriocins in lactic acid bacteria Nes,I.F.;D.B.Diep;L.S.Havarstein;M.B.Brurberg;V.Eijsink;H.Holo https://doi.org/10.1007/BF00395929
  38. J. Bacteriol. v.180 An exported inducer peptide regulates bacteriocin production in Enterococcus faecium CTC492 Nilsen,T.;I.F.Nes;H.Holo
  39. Regulation of pathogenicity in Staphylococcus aureus by a peptide-based density-sensing system;Cell-cell signaling in bacteria (1st ed.) Novick,R.P.;Dunny,G.M.(ed.);S.C.Winans(ed.)
  40. Appl. Environ. Microbiol v.65 Characterization and heterologous expression of the genes encoding enterocin a production, immunity, and regulation in Enterococcus faecium DPC1146 O'Keeffe,T.;C.Hill;R.P.Ross
  41. J. Bacteriol. v.178 Competence for genetic transformation in encapsulated strains of Streptococcus pneumoriae: two allelic variants of the peptide pheromone Pozzi,G.;L.Masala;F.Iannelli;R.Manganelli;L.S.Havarstein;L.Piccoli;D.Simon;D.A.Morrison https://doi.org/10.1128/jb.178.20.6087-6090.1996
  42. J. Biol. Chem. v.272 Effect of amino acid substitutions on the activity of carnobacteriocin B2. Overproduction of the antimicrobial peptide, its engineered variants, and its precursor in Escherochia coli Quadri,L.E.;L.Z.Yan;M.E.Stiles;J.C.Vederas https://doi.org/10.1074/jbc.272.6.3384
  43. J. Bacteriol. v.179 Characterization of a locus from Carnobacterium piscicola LV17B involved in bacteriocin production and immunity: evidence for global inducer-mediated transcriptional regulation Quadri,L.E.;M.Kleerebezem;O.P.Kuipers;W.M. de Vos;K.L.Roy;J.C.Vederas;M.E.Stiles https://doi.org/10.1128/jb.179.19.6163-6171.1997
  44. Antonie Van Leeuwenhoek v.82 Regulation of antimicrobial peptide production by autoinducer-mediated quorum sensing in lactic acid bacteria Quadri,L.E.N. https://doi.org/10.1023/A:1020624808520
  45. Food biopreservatives of microbial origin Ray,B.;M.Daeschel
  46. Mol. Gen. Genet v.259 Identification of the DNA-binding sites for two response regulators involved in control of bacteriocin synthesis in Lactobacillus plantarum C11 Risoen,P.A.;L.S.Havarstein;D.B.Diep;I.F.Nes
  47. Mol. Microbiol. v.37 Functional analysis of promoters involved in Lactobacillus Risoen,P.A.;M.B.Brurberg;V.G.Eijsink;I.F.Nes https://doi.org/10.1046/j.1365-2958.2000.02029.x
  48. Mol. Genet. Genomics. v.265 Regulation of bacteriocin production in Lactobacillus plantarum depends on a conserved promoter arrangement with consensus binding sequence Risoen,P.A.;O.Johnsborg;D.B.Diep;L.Hamoen;G.Venema;I.F.Nes https://doi.org/10.1007/s004380000397
  49. Antonie Van Leeuwenhoek v.76 Developing applications for lactococcal bacteriocins Ross,R.P.;M.Galvin;O.McAuliffe;S.M.Morgan;M.P.Ryan;D.P.Twomey;W.J.Meaney;C.Hill https://doi.org/10.1023/A:1002069416067
  50. Peptide antibiotics: discovery, modes of action and applications Peptide antibiotics: discovery,modes of action and applications Ryan,M.P.;C.Hill;R.P.Ross;C.J.Dutton(ed.);M.A.Haxell(ed.);A.I.McArthur(ed.);R.G.Wax(ed.)
  51. Adv. Biochem. Eng. Biotechnol v.68 Antimicrobial peptide of lactic acid bacteria: mode of action, genetics and biosynthesis Sablon,E.;B.Contreras;E.Vandamme
  52. J. Appl. Bacteriol. v.78 Induction of bacteriocin in Carnobacterium piscicola LV17 Saucier,L.;A.Poon;M.E.Stiles https://doi.org/10.1111/j.1365-2672.1995.tb03116.x
  53. Gene v.188 Transcriptional analysis and regulation of carnobacteriocin production in Carnobacterium pisicola LV17 Saucier,L.;A.S.Paradkar;L.S.Frost;S.E.Jensen;M.E.Stiles https://doi.org/10.1016/S0378-1119(96)00822-0
  54. Genes Dev. v.9 Converging sensing pathways mediate response to two extracellular compentnce factors in Bacillus subtilis Solomon,J.;A.Srivastava;R.Magnuson;A.D.Grossman https://doi.org/10.1101/gad.9.5.547
  55. Antonie Van Leeuwenhoek v.81 Cell to cell communication by autoinducing peptides in gram-positive bacteria Stume,M.H.;M.Kleerebezem;J.Nakayama;A.D.Akkermans;E.E.Vaugha;W.M. de Vos https://doi.org/10.1023/A:1020522919555
  56. Nat. Prod. Rep. v.17 Nonlantibiotic antibacterial peptides from lactic acid bacteria Van Belkum M.J.;M.E.Stiles https://doi.org/10.1039/a801347k
  57. J. Bacteriol. v.175 Characterization of the Lactococcus lactis nisin A operon genes nisP, encoding a subtilisin-like serine protease involved in precursor processing, and nisR, encoding a regulatory protein involved in nisin biosynthesis Van der Meer, J.R.;J.Polman;M.M.Beerthuyzen;R.J.Siezen;O.P.Kuipers;W.M. de Vos https://doi.org/10.1128/jb.175.9.2578-2588.1993
  58. Nat. Prod. Rep. v.16 Lantibiotics: biosynthesis, mode of action and applications Van Kraaij, C.;W.M. de Vos;R.J.Siezen;O.P.Kuipers https://doi.org/10.1039/a804531c
  59. Eur. J. Biochem. v.247 Influence of charge differences in the C-terminal part of nisin on antimicrobial activity and signaling capacity Van Kraaij, C.;E.Breukink;H.S.Rollema;R.J.Siezen;R.A.Demel;B. De Kruijff;O.P.Kuipers https://doi.org/10.1111/j.1432-1033.1997.00114.x
  60. Biochemistry v.38 Solution structure of carnobacteriocin B2 and implications for structure-activity relationships among type IIa bacteriocins from lactic acid bacteria Wang,Y.;M.E.Henz;N.L.Gallagher;S.Chai;A.C.Gibbs;L.Z.Yan;M.E.Stiles;D.S.Wishart;J.C.Vederas https://doi.org/10.1021/bi991351x
  61. FEMS Microbiol. Rev. v.25 Quorum-sensing in gram negative bacteria Whitehead,N.A.;A.M.Bamard;H.Slater;N.J.Simpson;G.P.Salmond https://doi.org/10.1111/j.1574-6976.2001.tb00583.x