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Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 233–243 | Cite as

Cell to cell communication by autoinducing peptides in gram-positive bacteria

  • Mark H.J. SturmeEmail author
  • Michiel Kleerebezem
  • Jiro Nakayama
  • Antoon D.L. Akkermans
  • Elaine E. Vaughan
  • Willem M. de Vos
Article

Abstract

While intercellular communication systems in Gram-negative bacteria are often based on homoserine lactones as signalling molecules, it has been shown that autoinducing peptides are involved in intercellular communication in Gram-positive bacteria. Many of these peptides are exported by dedicated systems, posttranslationally modified in various ways, and finally sensed by other cells via membrane-located receptors that are part of two-component regulatory systems. In this way the expression of a variety of functions including virulence, genetic competence and the production of antimicrobial compounds can be modulated in a co-ordinated and cell density- and growth phase-dependent manner. Occasionally the autoinducing peptide has a dual function, such as in the case of nisin that is both a signalling pheromone involved in quorum sensing and an antimicrobial peptide. Moreover, biochemical, genetic and genomic studies have shown that bacteria may contain multiple quorum sensing systems, underlining the importance of intercellular communication. Finally, in some cases different peptides may be recognised by the same receptor, while also hybrid receptors have been constructed that respond to new peptides or show novel responses. This paper provides an overview of the characteristics of autoinducing peptide-based quorum sensing systems, their application in various gram-positive bacteria, and the discovery of new systems in natural and engineered ecosystems.

autoinducing peptides Gram-positive bacteria quorum sensing two-component regulatory systems 

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References

  1. Ansaldi M, Marolt D, Stebe T, Mandic-Mulec I & Dubnau D (2002) Specific activation of the Baciullus quorum-sensing systems by isoprenylated pheromone variants. Mol. Microbiol. 44: 1561–1573.PubMedCrossRefGoogle Scholar
  2. Bacon-Schneider K, Palmer TM & Grossman AD (2002) Characterization of comQ and comX, two genes required for production of ComX pheromone on Bacillus subtilis. J. Bacteriol. 184: 410–419.PubMedCrossRefGoogle Scholar
  3. Béjà O, Suzuki MT, Koonin EV, Aravind L, Hadd A, Nguyen LP, Villacorta R, Amjadi M, Garrigues C, Jovanovich SB, Feldman RA & DeLong EF (2000) Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environ. Microbiol. 2: 516–529.PubMedCrossRefGoogle Scholar
  4. Berka RM, Hahn J, Albano M, Draskovic I, Persuh M, Cui X, Sloma A, Widner W & Dubnau D (2002) Microarray analysis of the Bacillus subtilis K-state: genome-wide expression changes dependent on ComK Mol. Microbiol. 43: 1331–1345.PubMedCrossRefGoogle Scholar
  5. Brurberg MB, Nes IF & Eijsink VGH (1997) Pheromone-induced production of antimicrobial peptides in Lactobacillus. Mol.Microbiol. 26: 347–360.PubMedCrossRefGoogle Scholar
  6. Bryan EM, Bae T, Kleerebezem M & Dunny GM (2000) Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 44: 183–190.PubMedCrossRefGoogle Scholar
  7. Cheng Q, Campbell EA, Naughton AM, Johnson S & Masure HR (1997) The com locus controls genetic transformation in Streptococcus pneumoniae. Mol. Microbiol. 23: 683–692.PubMedCrossRefGoogle Scholar
  8. Dabard J, Bridonneau C, Phillipe C, Anglade P, Molle D, Nardi M, Ladiré M, Girardin H, Marcille F, Gomez A & Fons M (2001) Ruminococcin A, a new lantibiotic produced by a Ruminococcus gnavus strain isolated from human feces. Appl. Environ. Microbiol. 67: 4111–4118.PubMedCrossRefGoogle Scholar
  9. De Ruyter PGGA, Kuipers OP & de Vos WM (1996) Controlled gene expression systems for Lactococcus lactis with the foodgrade inducer nisin. Appl. Environ. Microbiol. 62: 3662–3667.PubMedGoogle Scholar
  10. De Saizieu A, Gardès C, Flint N, Wagner C, Kamber M, Mitchell TJ, Keck 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.PubMedCrossRefGoogle Scholar
  11. De Vos WM, Kuipers OP, van der Meer JR & Siezen RJ (1995) Maturation pathway of nisin and other lantibiotics: post-translationally modified antimicrobial peptides exported by Gram-positive bacteria. Mol. Microbiol. 17: 427–437.PubMedGoogle Scholar
  12. De Vos WM, Kleerebezem M & Kuipers OP (1997) Expression systems for industrial Gram-positive bacteria with low guanine and cytosine content. Curr. Opin. Microbiol. 8: 547–553.Google Scholar
  13. 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.PubMedGoogle Scholar
  14. Dufour P, Jarraud S, Vandenesch F, Greenland T, Novick RP, Bes M, Etienne J & Lina G (2002) High genetic variability of the agr locus in Staphylococcus species. J. Bacteriol. 184: 1180–1186.PubMedCrossRefGoogle Scholar
  15. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellog G, Wu S, Brown EL, Zagursky RJ, Shlaes D & Projan SJ (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J. Bacteriol. 183: 7341–7353.PubMedCrossRefGoogle Scholar
  16. Eberl L, Winson MK, Sternberg C, Stewart GSAB, Christiansen G, Chhabra SR, Bycroft B, Williams P, Molin S & Givskov M (1996) Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20: 127–136.PubMedGoogle Scholar
  17. Eichenbaum Z, Federle MJ, Marra D, de Vos WM, Kleerebezem M & Scott JR (1998) Use of the lactococcal nisA promoter to regulate gene expression in gram-positive bacteria: comparison of induction level and promoter strength. Appl. Environ. Microbiol. 64: 2763–2769.PubMedGoogle Scholar
  18. Ennahar S, Sashihara T, Sonomoto K & Ishizaki A (2000) Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24: 85–106.PubMedCrossRefGoogle Scholar
  19. Fuqua WC, Winans SC & Greenberg EP (1994) Quorum-sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269–275.PubMedGoogle Scholar
  20. Gao FH, Abee T & Konings WN (1991) Mechanism of action of the peptide antibiotic nisin in liposomes and cytochrome c oxidase-containing proteoliposomes. Appl. Environ. Microbiol. 57: 2164–2170.PubMedGoogle Scholar
  21. Gomez A, Ladiré M, Marcille F & Fons M (2002) Trypsin mediates growth phase-dependent transcriptional regulation of genes involved in biosynthesis of ruminococcin A, a lantibiotic produced by a Ruminococcus gnavus strain from a human intestinal microbiota. J. Bacteriol. 184: 18–28.PubMedCrossRefGoogle Scholar
  22. Gray KM, Pearson JP, Downie JA, Boboye BE & Greenberg EP (1996) Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178: 372–376.PubMedGoogle Scholar
  23. Grebe TW & Stock JB (1999) The histidine protein kinase superfamily. Adv. Microb. Physiol. 41: 139–227.PubMedCrossRefGoogle Scholar
  24. Haas W, Shepard BD & Gilmore MS (2002) Two-component regulator of Enterococcus faecalis cytolysin responds to quorumsensing autoinduction. Nature 415: 84–87.PubMedCrossRefGoogle Scholar
  25. Håvarstein LS, Diep DB & Nes IF (1995a) A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol. Microbiol. 16: 229–240.PubMedGoogle Scholar
  26. Håvarstein LS, Coomaraswamy G & Morrison DA (1995b) An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 92: 11140–11144.PubMedCrossRefGoogle Scholar
  27. Håvarstein LS, Hakenbeck R & Gaustad P (1997) Natural competence in the genus Streptococcus: evidence that streptococci can change pherotype by interspecies recombinational exchanges. J. Bacteriol. 179: 6589–6594.PubMedGoogle Scholar
  28. Holden M, Swift S & Williams P (2000) New signal molecules on the quorum-sensing block. Trends Microbiol. 8: 101–103.PubMedCrossRefGoogle Scholar
  29. Jarraud S, Lyon GJ, Figueiredo AMS, Gérard L, Vandenesch F, Etienne J, Muir TW & Novick RP (2000) Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J. Bacteriol. 182: 6517–6522.PubMedCrossRefGoogle Scholar
  30. Ji G, Beavis R & Novick RP (1997) Bacterial interference caused by autoinducing peptide variants. Science 276: 2027–2030.PubMedCrossRefGoogle Scholar
  31. Jiang M, Grau R & Perego M (2000) Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis. J. Bacteriol. 182: 303–310.PubMedCrossRefGoogle Scholar
  32. Kalmokoff ML & Teather RM (1997) Isolation and characterization of a bacteriocin (butyrivibriocin AR10) from the ruminal anaerobe Butyrivibrio fibrisolvens AR10: evidence in support of the widespread occurrence of bacteriocin-like activity among ru242 minal isolates of B. fibrisolvens. Appl. Environ. Microbiol. 63: 394–402.PubMedGoogle Scholar
  33. Kalmokoff ML, Lu D, Whitford MF & Teather RM (1999) Evidence for production of a new lantibiotic (butyrivibriocin OR79A) by the ruminal anaerobe Butyrivibrio fibrisolvens OR79: characterization of the structural gene encoding butyrivibriocin OR79A. Appl. Environ. Microbiol. 65: 2128–2135.PubMedGoogle Scholar
  34. Kleerebezem M, Quadri LEN, Kuipers OP & de Vos WM (1997a) Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol. Microbiol. 24: 895–904.PubMedCrossRefGoogle Scholar
  35. Kleerebezem M, Beerthuyzen MM, Vaughan EE, de Vos WM & Kuipers OP (1997b) Controlled gene expression systems for lactic acid bacteria: transferable nisin-inducible expression cassettes for Lactococcus, Leuconostoc, and Lactobacillus spp. Appl. Environ. Microbiol. 63: 4581–4584.PubMedGoogle Scholar
  36. Kleerebezem M, de Vos WM & Kuipers OP (1999) The lantibiotics nisin and subtilin act as extracellular regulators of their own biosynthesis. In: Dunny GM & Winans SC (Eds) Cell- Cell Signaling in Bacteria (pp 159–174). American Society for Microbiology Press, Washington D.C.Google Scholar
  37. Kleerebezem M, Kuipers OP, de Vos WM, Stiles ME & Quadri LEN (2001a) A two-component signal transduction cascade in Carnobacterium piscicola LV17B: two signalling peptides and one sensor-transmitter. Peptides 22: 1597–1601.PubMedCrossRefGoogle Scholar
  38. Kleerebezem M & Quadri LEN (2001b) Peptide pheromonedependent regulation of antimicrobial peptide production in Gram-positive bacteria; a case of multicellular behavior. Peptides 22: 1579–1596.PubMedCrossRefGoogle Scholar
  39. Kleerebezem M, Bongers R, Rutten G, de Vos WM & uipers OP (2002) Autoregulation of subtilin biosynthesis: identification of conserved pentanucleotide direct repeats, essential for subtilin mediated spa promoter regulation, submitted.Google Scholar
  40. Klein C, Kaletta C, Schnell N & Entian KD (1992) Analysis of genes involved in biosynthesis of the lantibiotic subtilin. Appl. Environ. Microbiol. 58: 132–142.PubMedGoogle Scholar
  41. Kuipers OP, Beerthuyzen MM, de Ruyter GGA, Luesink EJ & de Vos WM (1995) Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J. Biol. Chem. 270: 27299–27304.PubMedCrossRefGoogle Scholar
  42. Kuipers OP, de Ruyter PGGA, Kleerebezem M & de Vos WM (1997) Controlled overproduction of proteins by lactic acid bacteria. Trends Biotechnol. 15: 135–140.PubMedCrossRefGoogle Scholar
  43. Lange R, Wagner C, de Saizieu A, Flint N, Molnos J, Stieger M, Caspers P, Kamber M, Keck W & Amrein KE (1999) Domain organization and molecular characterization of 13 two-component systems identified by genome sequencing of Streptococcus pneumoniae. Gene 237: 223–234.PubMedCrossRefGoogle Scholar
  44. Lazazzera BA, Palmer T, Quisel J & Grossman AD (1999) Cell density control of gene expression and development in Bacillus subtilis. In: Dunny GM & Winans SC (Eds) Cell-Cell Signaling in Bacteria (pp 27–46). American Society for Microbiology Press, Washington D.C.Google Scholar
  45. Lorenz MG & Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58: 563–602.PubMedGoogle Scholar
  46. Lyon GJ, Mayville P, Muir TW & Novick RP (2000) Rational design of a global inhibitor of the virulence response in Staphylococcus aureus, based in part on localization of the site of inhibition to the receptor-histidine kinase, AgrC. Proc. Natl. Acad. Sci. USA 97: 13330–13335.PubMedCrossRefGoogle Scholar
  47. Lyon GJ, Wright JS, Christopoulos A, Novick RP & Muir TW (2002) Reversible and specific extracellular antagonism of receptor-histidine-kinase signaling. J. Biol. Chem. 277: 6247–6253.PubMedCrossRefGoogle Scholar
  48. Magnuson R, Solomon J & Grossman AD (1994) Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77: 207–216.PubMedCrossRefGoogle Scholar
  49. McAuliffe O, Ross RP & Hill C (2001) Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiol. Rev. 25: 285–308.PubMedCrossRefGoogle Scholar
  50. McDowell P, Affas Z, Reynolds C, Holden MTG, Wood SJ, Saint S, Cockayne A, Hill PJ, Dodd CER, Bycroft BW, Chan WC & Williams P (2001) Structure, activity and evolution of the group I thiolactone peptide quorum-sensing system of Staphylococcus aureus. Mol. Microbiol. 41: 503–512.CrossRefGoogle Scholar
  51. MacNeil IA, Tiong CL, Minor C, August PR, Grossman TH, Loiacono KA, Lynch BA, Phillips T, Narula S, Sundaramoorthi R, Tyler A, Aldredge T, Long H, Gilman M, Holt D & Osburne MS (2001) Expression and isolation of antimicrobial small molecules from soil DNA libraries. J. Mol. Microbiol. Biotechnol. 3: 301–308.PubMedGoogle Scholar
  52. Mayville P, Ji G, Beavis R, Yang H, Goger M, Novick R & Muir TW (1999) Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl. Acad. Sci. USA 96: 1218–1223.PubMedCrossRefGoogle Scholar
  53. McQuade RS, Comella N & Grossman AD (2001) Control of a family of phosphatase regulatory genes (phr) by the alternate sigma factor sigma-H of Bacillus subtilis. J. Bacteriol. 183: 4905–4909.PubMedCrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. Morel-Deville F, Ehrlich SD & Morel P (1997) Identification by PCR of genes encoding multiple response regulators. Microbiology 143: 1513–1520.PubMedCrossRefGoogle Scholar
  56. Nakayama J, Cao Y, Horii T, Sakuda S, Akkermans ADL, de Vos WM & Nagasawa H (2001) Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol. Microbiol. 41: 145–154.PubMedCrossRefGoogle Scholar
  57. Nakayama J, Akkermans ADL & de Vos WM (2002) Genomic survey of two-component regulatory systems putatively involved in peptide pheromone mediated quorum sensing of low G+C gram-positive bacteria, submitted.Google Scholar
  58. 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 Press, Washington D.C.Google Scholar
  59. Nilsen T, Nes IF & Holo H (1998) An exported inducer peptide regulates bacteriocin production in Enterococcus faecium CTC492. J. Bacteriol. 180: 1848–1854.PubMedGoogle Scholar
  60. Novick RP (1999) Regulation of pathogenicity in Staphylococcus aureus by a peptide-based density-sensing system. In: Dunny GM & Winans SC (Eds) Cell-Cell Signaling in Bacteria (pp 129–146). American Society for Microbiology Press, Washington D.C.Google Scholar
  61. O'Connell-Motherway M, van Sinderen D, Morel-Deville F, Fitzgerald GF, Ehrlich SD & Morel P (2000) Six putative two-component regulatory systems isolated from Lactococcus lactis subsp. cremoris MG1363. Microbiology 146: 935–947.PubMedGoogle Scholar
  62. Otto M, Echner H, Voelter W & Götz F (2001) Pheromone crossinhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 69: 1957–1960.PubMedCrossRefGoogle Scholar
  63. Parkinson JS (1995) Genetic approaches for signaling pathways and proteins. In: Hoch JA & Silhavy TJ (Eds) Two-Component Signal Transduction (pp 9–23). American Society for Microbiology Press, Washington D.C.Google Scholar
  64. Pavan S, Hols P, Delcour J, Geoffroy MC, Grangette C, Kleerebezem M & Mercenier A (2000) Adaptation of the nisincontrolled expression system in Lactobacillus plantarum: a tool to study in vivo biological effects. Appl. Environ. Microbiol. 66: 4427–4432.PubMedCrossRefGoogle Scholar
  65. Perego M (1999) Self-signaling by Phr peptides modulates Bacillus subtilis development. In: Dunny GM & Winans SC (Eds) Cell- Cell Signaling in Bacteria (pp 243–258). American Society for Microbiology Press, Washington D.C.Google Scholar
  66. Quadri LEN, Kleerebezem M, Kuipers OP, de Vos WM, Roy KL, Vederas JC & Stiles ME (1997) Characterization of a locus from Carnobacterium piscicola LV17B involved in bacteriocin production and immunity: evidence for global inducer-mediated transcriptional regulation. J. Bacteriol. 179: 6163–6171.PubMedGoogle Scholar
  67. 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.PubMedCrossRefGoogle Scholar
  68. Rondon MR, August PR, Betterman AD, Brady SF, Grossman TH, Liles MR, Loiacono KA, Lynch BA, MacNeil IA, Minor C, Tiong CL, Gilman m, Osburne MS, Clardy J, Handelsman J & Goodman RM (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66: 2541–2547.PubMedCrossRefGoogle Scholar
  69. Rondon MR, Raffel SJ, Goodman RM & Handelsman J (1999) Toward functional genomics in bacteria: Analysis of gene expression in Escherichia coli from a bacterial artificial chromosome library of Bacillus cereus. Proc. Natl. Acad. Sci. USA 96: 6451–6455.PubMedCrossRefGoogle Scholar
  70. Saenz HL, Augsburger V, Vuong C, Jack RW, Götz F & Otto M (2000) Inducible expression and cellular location of AgrB, a protein involved in the maturation of the staphylococcal quorum-sensing pheromone. Arch. Microbiol. 174: 452–455.PubMedCrossRefGoogle Scholar
  71. Singh P, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ & Greenberg EP (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407: 762–764.PubMedCrossRefGoogle Scholar
  72. Swift S, Vaughan EE & de Vos WM (2000) Quorum sensing within the gut ecosystem. Microbial Ecol. Health Dis. 12: 81–92.CrossRefGoogle Scholar
  73. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, Peterson S, Heidelberg J, DeBoy RT, Haft DH, Dodson RJ, Durkin AS, Gwinn M, Kolonay JF, Nelson WC, Peterson JD, Umayam LA, White O, Salzberg SL, Lewis MR, Radune D, Holtzapple E, Khouri H, Wolf AM, Utterback TR, Hansen CL, McDonald LA, Feldblyum TV, Angiuoli S, Dickinson T, Hickey EK, Holt IE, Loftus BJ, Yang F, Smith HO, Venter JC, Dougherty BA, Morrison DA, Hollingshead SK & Fraser CM (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498–506.PubMedCrossRefGoogle Scholar
  74. Throup JP, Koretke KK, Bryant AP, Ingraham KA, Chalker AF, Ge Y, Marra A, Wallis NG, Brown JR, Holmes DJ, Rosenberg M & Burnham MKR (2000) A genomic analysis of two-component signal transduction in Streptococcus pneumoniae. Mol. Microbiol. 35: 566–576.PubMedCrossRefGoogle Scholar
  75. Tortosa P & Dubnau D (1999) Competence for transformation: a matter of taste. Curr. Opin. Microbiol. 2: 588–592.PubMedCrossRefGoogle Scholar
  76. Tortosa P, Logsdon L, Kraigher B, Itoh Y, Mandic-Mulec I & Dubnau D (2001) Specificity and genetic polymorphism of the Bacillus competence quorum-sensing system. J. Bacteriol. 183: 451–460.PubMedCrossRefGoogle Scholar
  77. Upton M, Tagg JR, Wescombe P & Jenkinson HF (2001) Intra and interspecies signaling between Streptococcus salivarius and Streptococcus pyogenes mediated by SalA and SalA1 lantibiotic peptides. J. Bacteriol. 183: 3931–3938.PubMedCrossRefGoogle Scholar
  78. Van der Meer JR, Polman J, Beerthuyzen MM, Siezen RJ, Kuipers OP & De Vos WM (1993) 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. J. Bacteriol. 175: 2578–2588.PubMedGoogle Scholar
  79. Van Kraaij C, Breukink E, Noordermeer MA, Demel RA, Siezen RJ, Kuipers OP & de Kruijff B (1998) Pore formation by nisin involves translocation of its C-terminal part across the membrane. Biochemistry 37: 16033–16040.PubMedCrossRefGoogle Scholar
  80. Whatmore AM, Barcus VA & Dowson CG (1999) Genetic diversity of the streptococcal competence (com) gene locus. J. Bacteriol. 181: 3144–3154.PubMedGoogle Scholar
  81. Whitehead NA, Barnard AML, Slater H, Simpson NJL & Salmond GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25: 365–404.PubMedCrossRefGoogle Scholar
  82. Winson MK, Camara M, Latifi A, Fogliono M, Chhabra SR, Daykin M, Bally M, Chapon V, Salmond GPC, Bycroft BW, Lazdunski A, Stewart GSAB & Williams P (1995) Multiple N-Acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92: 9427–9431.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Mark H.J. Sturme
    • 1
    Email author
  • Michiel Kleerebezem
    • 2
    • 3
  • Jiro Nakayama
    • 4
  • Antoon D.L. Akkermans
    • 1
  • Elaine E. Vaughan
    • 1
    • 3
  • Willem M. de Vos
    • 1
    • 3
  1. 1.Laboratory of MicrobiologyWageningen UniversityWageningenthe Netherlands
  2. 2.NIZO Food ResearchEde, the Netherlands
  3. 3.Wageningen Centre for Food SciencesWageningenthe Netherlands
  4. 4.Department of Bioscience and Biotechnology, Faculty of AgricultureKyushu UniversityHigashi-ku, FukuokaJapan

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