Skip to main content
SpringerLink
Log in

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

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Brurberg MB, Nes IF & Eijsink VGH (1997) Pheromone-induced production of antimicrobial peptides in Lactobacillus. Mol.Microbiol. 26: 347–360.

    Article  PubMed  CAS  Google Scholar 

  • Bryan EM, Bae T, Kleerebezem M & Dunny GM (2000) Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 44: 183–190.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Ennahar S, Sashihara T, Sonomoto K & Ishizaki A (2000) Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24: 85–106.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Grebe TW & Stock JB (1999) The histidine protein kinase superfamily. Adv. Microb. Physiol. 41: 139–227.

    Article  PubMed  CAS  Google Scholar 

  • Haas W, Shepard BD & Gilmore MS (2002) Two-component regulator of Enterococcus faecalis cytolysin responds to quorumsensing autoinduction. Nature 415: 84–87.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Holden M, Swift S & Williams P (2000) New signal molecules on the quorum-sensing block. Trends Microbiol. 8: 101–103.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ji G, Beavis R & Novick RP (1997) Bacterial interference caused by autoinducing peptide variants. Science 276: 2027–2030.

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Grau R & Perego M (2000) Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis. J. Bacteriol. 182: 303–310.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kuipers OP, de Ruyter PGGA, Kleerebezem M & de Vos WM (1997) Controlled overproduction of proteins by lactic acid bacteria. Trends Biotechnol. 15: 135–140.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Lorenz MG & Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58: 563–602.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Magnuson R, Solomon J & Grossman AD (1994) Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77: 207–216.

    Article  PubMed  CAS  Google Scholar 

  • McAuliffe O, Ross RP & Hill C (2001) Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiol. Rev. 25: 285–308.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Morel-Deville F, Ehrlich SD & Morel P (1997) Identification by PCR of genes encoding multiple response regulators. Microbiology 143: 1513–1520.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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 

  • Nilsen T, Nes IF & Holo H (1998) An exported inducer peptide regulates bacteriocin production in Enterococcus faecium CTC492. J. Bacteriol. 180: 1848–1854.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Otto M, Echner H, Voelter W & Götz F (2001) Pheromone crossinhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 69: 1957–1960.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Swift S, Vaughan EE & de Vos WM (2000) Quorum sensing within the gut ecosystem. Microbial Ecol. Health Dis. 12: 81–92.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Tortosa P & Dubnau D (1999) Competence for transformation: a matter of taste. Curr. Opin. Microbiol. 2: 588–592.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Whatmore AM, Barcus VA & Dowson CG (1999) Genetic diversity of the streptococcal competence (com) gene locus. J. Bacteriol. 181: 3144–3154.

    PubMed  CAS  Google Scholar 

  • Whitehead NA, Barnard AML, Slater H, Simpson NJL & Salmond GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25: 365–404.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Microbiology, Wageningen University, Hesselink van Suchtelenweg 4, 6703 CT, Wageningen, the Netherlands

    Mark H.J. Sturme, Antoon D.L. Akkermans, Elaine E. Vaughan & Willem M. de Vos

  2. NIZO Food Research, Kernhemseweg 2, PO Box 20, 6710 BA, Ede, the Netherlands

    Michiel Kleerebezem

  3. Wageningen Centre for Food Sciences, Wageningen, the Netherlands

    Michiel Kleerebezem, Elaine E. Vaughan & Willem M. de Vos

  4. Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka, 812-8581, Japan

    Jiro Nakayama

Authors
  1. Mark H.J. Sturme
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michiel Kleerebezem
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiro Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antoon D.L. Akkermans
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elaine E. Vaughan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Willem M. de Vos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark H.J. Sturme.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sturme, M.H., Kleerebezem, M., Nakayama, J. et al. Cell to cell communication by autoinducing peptides in gram-positive bacteria. Antonie Van Leeuwenhoek 81, 233–243 (2002). https://doi.org/10.1023/A:1020522919555

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020522919555

Search

Navigation