Biofilms: Maintenance, Development, and Disassembly of Bacterial Communities Are Determined by QS Cascades

  • Hadas Ganin
  • Eliane Hadas Yardeni
  • Ilana Kolodkin-GalEmail author


Unicellular organisms use a variety of mechanisms to coordinate activity within communities, called biofilms, and across species to accomplish complex multicellular processes (Aguilar et al., Curr Opin Microbiol 10:638–643, 2007; Kolter and Greenberg, Nature 441:300–302, 2006; Miller and Bassler, Annu Rev Microbiol 55:165–199, 2001; Stoodley et al., Annu Rev Microbiol 56:187–209, 2002). Informed by chemical communication, motile cells of the Bacillus subtilis and filamentous cells of the Streptomycetes organize themselves into conspicuous multicellular structures that carry out specialized tasks in spore formation and dispersal. Furthermore, most bacteria have evolved elaborate mechanisms for adhering to solid surfaces and thereby establishing complex communities referred to as biofilms. Importantly, QS cascades are essential for the formation of bacterial multicellular communities and complex biofilms. This chapter focuses on the major QS systems, playing an active role in the rise of complex bacterial communities in different bacterial models.


Vibrio Species Pseudomonas Quinolone Signal Surfactin Producer Toxin Coregulated Pilus Multicellular Community 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aguilar C, Vlamakis H, Losick R, Kolter R (2007) Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10:638–643PubMedPubMedCentralGoogle Scholar
  2. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–1128PubMedGoogle Scholar
  3. Arima K, Kakinuma A, Tamura G (1968) Surfactin a crystalline peptidelipid surfactant produced by Bacillus Subtilis – isolation characterization and its inhibition of fibrin clot formation. Biochem Biophys Res Commun 31:488–494Google Scholar
  4. Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102:11076–11081PubMedPubMedCentralGoogle Scholar
  5. Baron SS, Rowe JJ (1981) Antibiotic action of pyocyanin. Antimicrob Agents Chemother 20:814–820PubMedPubMedCentralGoogle Scholar
  6. Bassler BL, Losick R (2006) Bacterially speaking. Cell 125:237–246PubMedGoogle Scholar
  7. Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A 110:E1621–1630PubMedPubMedCentralGoogle Scholar
  8. Bjarnsholt T, Jensen PO, Burmolle M, Hentzer M, Haagensen JAJ, Hougen HP, Calum H, Madsen KG, Moser C, Molin S et al (2005) Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373–383PubMedGoogle Scholar
  9. Boles BR, Horswill AR (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052PubMedPubMedCentralGoogle Scholar
  10. Boles BR, Horswill AR (2011) Staphylococcal biofilm disassembly. Trends Microbiol 19:449–455PubMedPubMedCentralGoogle Scholar
  11. Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 98:11621–11626PubMedPubMedCentralGoogle Scholar
  12. Branda SS, Gonzalez-Pastor JE, Dervyn E, Ehrlich SD, Losick R, Kolter R (2004) Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186:3970–3979PubMedPubMedCentralGoogle Scholar
  13. Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229–1238PubMedGoogle Scholar
  14. Britigan BE, Roeder TL, Rasmussen GT, Shasby DM, McCormick ML, Cox CD (1992) Interaction of the Pseudomonas aeruginosa secretory products pyocyanin and pyochelin generates hydroxyl radical and causes synergistic damage to endothelial cells. Implications for Pseudomonas-associated tissue injury. J Clin Invest 90:2187–2196PubMedPubMedCentralGoogle Scholar
  15. Bryers JD (2008) Medical biofilms. Biotechnol Bioeng 100:1–18PubMedPubMedCentralGoogle Scholar
  16. Cha M, Hong S, Kang MY, Lee JW, Jang J (2012) Gas-phase removal of biofilms from various surfaces using carbon dioxide aerosols. Biofouling 28:681–686PubMedGoogle Scholar
  17. Chai Y, Chu F, Kolter R, Losick R (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67:254–263PubMedPubMedCentralGoogle Scholar
  18. Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo JH, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85:418–430PubMedPubMedCentralGoogle Scholar
  19. Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo JH (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15:848–864PubMedPubMedCentralGoogle Scholar
  20. Collier DN, Anderson L, McKnight SL, Noah TL, Knowles M, Boucher R, Schwab U, Gilligan P, Pesci EC (2002) A bacterial cell to cell signal in the lungs of cystic fibrosis patients. Fems Microbiol Lett 215:41–46PubMedGoogle Scholar
  21. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464PubMedGoogle Scholar
  22. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322PubMedGoogle Scholar
  23. Dai L, Yang L, Parsons C, Findlay VJ, Molin S, Qin ZQ (2012) Staphylococcus epidermidis recovered from indwelling catheters exhibit enhanced biofilm dispersal and “self-renewal” through downregulation of agr. BMC Microbiol 12:102PubMedPubMedCentralGoogle Scholar
  24. Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036PubMedPubMedCentralGoogle Scholar
  25. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298PubMedGoogle Scholar
  26. De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH (2001) Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67:1865–1873PubMedPubMedCentralGoogle Scholar
  27. Deziel E, Gopalan S, Tampakaki AP, Lepine F, Padfield KE, Saucier M, Xiao G, Rahme LG (2005) The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol 55:998–1014PubMedGoogle Scholar
  28. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK (2006) The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61:1308–1321PubMedGoogle Scholar
  29. Dietrich LE, Teal TK, Price-Whelan A, Newman DK (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203–1206PubMedPubMedCentralGoogle Scholar
  30. Dietrich LE, Okegbe C, Price-Whelan A, Sakhtah H, Hunter RC, Newman DK (2013) Bacterial community morphogenesis is intimately linked to the intracellular redox state. J Bacteriol 195:1371–1380PubMedPubMedCentralGoogle Scholar
  31. Diggle SP, Winzer K, Chhabra SR, Worrall KE, Camara M, Williams P (2003) The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29–43PubMedGoogle Scholar
  32. Diggle SP, Stacey RE, Dodd C, Camara M, Williams P, Winzer K (2006) The galactophilic lectin, LecA, contributes to biofilm development in Pseudomonas aeruginosa. Environ Microbiol 8:1095–1104PubMedGoogle Scholar
  33. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449PubMedGoogle Scholar
  34. Ellermeier CD, Hobbs EC, Gonzalez-Pastor JE, Losick R (2006) A three-protein signaling pathway governing immunity to a bacterial cannibalism toxin. Cell 124:549–559PubMedGoogle Scholar
  35. Engebrecht J, Nealson K, Silverman M (1983) Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32:773–781PubMedGoogle Scholar
  36. Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2:e135PubMedPubMedCentralGoogle Scholar
  37. Faruque SM, Albert MJ, Mekalanos JJ (1998) Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62:1301PubMedPubMedCentralGoogle Scholar
  38. Foreman A, Jervis-Bardy J, Boase SJ, Tan L, Wormald PJ (2013) Noninvasive Staphylococcus aureus biofilm determination in chronic rhinosinusitis by detecting the exopolysaccharide matrix component poly-N-acetylglucosamine. Int Forum Allergy Rhinol 3:83–88PubMedGoogle Scholar
  39. Fujita M, Gonzalez-Pastor JE, Losick R (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187:1357–1368PubMedPubMedCentralGoogle Scholar
  40. Glasser NR, Kern SE, Newman DK (2014) Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosa by facilitating generation of ATP and a proton-motive force. Mol Microbiol 92:399–412PubMedGoogle Scholar
  41. Gonzalez-Pastor JE, Hobbs EC, Losick R (2003) Cannibalism by sporulating bacteria. Science 301:510–513PubMedGoogle Scholar
  42. Guina T, Purvine SO, Yi EC, Eng J, Goodlett DR, Aebersold R, Miller SI (2003) Quantitative proteomic analysis indicates increased synthesis of a quinolone by Pseudomonas aeruginosa isolates from cystic fibrosis airways. Proc Natl Acad Sci U S A 100:2771–2776PubMedPubMedCentralGoogle Scholar
  43. Ha C, Park SJ, Im SJ, Park SJ, Lee JH (2012) Interspecies signaling through QscR, a quorum receptor of Pseudomonas aeruginosa. Mol Cells 33:53–59PubMedPubMedCentralGoogle Scholar
  44. Hammer BK, Bassler BL (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50:101–104PubMedGoogle Scholar
  45. Hays EE, Wells IC, Katzman PA, Cain CK, Jacobs FA, Thayer SA, Doisy EA, Gaby WL, Roberts EC, Muir RD et al (1945) Antibiotic substances produced by Pseudomonas Aeruginosa. J Biol Chem 159:725–750Google Scholar
  46. Henke JM, Bassler BL (2004) Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186:6902–6914PubMedPubMedCentralGoogle Scholar
  47. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Hoiby N et al (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87–102PubMedGoogle Scholar
  48. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P et al (2003a) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815PubMedPubMedCentralGoogle Scholar
  49. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P et al (2003b) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815PubMedPubMedCentralGoogle Scholar
  50. Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883PubMedGoogle Scholar
  51. Kearns DB, Chu F, Branda SS, Kolter R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55:739–749PubMedGoogle Scholar
  52. Kelly RC, Bolitho ME, Higgins DA, Lu W, Ng WL, Jeffrey PD, Rabinowitz JD, Semmelhack MF, Hughson FM, Bassler BL (2009) The Vibrio cholerae quorum-sensing autoinducer CAI-1: analysis of the biosynthetic enzyme CqsA. Nat Chem Biol 5:891–895PubMedPubMedCentralGoogle Scholar
  53. Kempes CP, Okegbe C, Mears-Clarke Z, Follows MJ, Dietrich LE (2014) Morphological optimization for access to dual oxidants in biofilms. Proc Natl Acad Sci U S A 111:208–213PubMedPubMedCentralGoogle Scholar
  54. Kirisits MJ, Parsek MR (2006) Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities? Cell Microbiol 8:1841–1849PubMedGoogle Scholar
  55. Kluge B, Vater J, Salnikow J, Eckart K (1988) Studies on the biosynthesis of surfactin, a lipopeptide antibiotic from Bacillus-subtilis Atcc-21332. FEBS Lett 231:107–110PubMedGoogle Scholar
  56. Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S, Givskov M (2005) The LuxR receptor: the sites of interaction with quorum-sensing signals and inhibitors. Microbiology 151:3589–3602PubMedGoogle Scholar
  57. Kolodkin-Gal I, Elsholz AK, Muth C, Girguis PR, Kolter R, Losick R (2013) Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase. Genes Dev 27:887–899PubMedPubMedCentralGoogle Scholar
  58. Kolter R, Greenberg EP (2006) Microbial sciences: the superficial life of microbes. Nature 441:300–302PubMedGoogle Scholar
  59. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A (1996) A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21:1137–1146PubMedGoogle Scholar
  60. Lau GW, Hassett DJ, Ran H, Kong F (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10:599–606PubMedGoogle Scholar
  61. Ledgham F, Ventre I, Soscia C, Foglino M, Sturgis JN, Lazdunski A (2003) Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol Microbiol 48:199–210PubMedGoogle Scholar
  62. Lee SH, Hava DL, Waldor MK, Camilli A (1999) Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99:625–634PubMedGoogle Scholar
  63. Lepine F, Deziel E, Milot S, Rahme LG (2003) A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseudomonas aeruginosa cultures. Biochim Biophys Acta 1622:36–41PubMedGoogle Scholar
  64. Lequette Y, Greenberg EP (2005) Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37–44PubMedPubMedCentralGoogle Scholar
  65. Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188:3365–3370PubMedPubMedCentralGoogle Scholar
  66. Lintz MJ, Oinuma K, Wysoczynski CL, Greenberg EP, Churchill ME (2011) Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc Natl Acad Sci U S A 108:15763–15768PubMedPubMedCentralGoogle Scholar
  67. Lombardia E, Rovetto AJ, Arabolaza AL, Grau RR (2006) A LuxS-dependent cell-to-cell language regulates social behavior and development in Bacillus subtilis. J Bacteriol 188:4442–4452PubMedPubMedCentralGoogle Scholar
  68. Lopez D, Fischbach MA, Chu F, Losick R, Kolter R (2009a) Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc Natl Acad Sci U S A 106:280–285PubMedPubMedCentralGoogle Scholar
  69. Lopez D, Vlamakis H, Kolter R (2009b) Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33:152–163PubMedGoogle Scholar
  70. Lopez D, Vlamakis H, Losick R, Kolter R (2009c) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74:609–618PubMedPubMedCentralGoogle Scholar
  71. Lopez D, Vlamakis H, Losick R, Kolter R (2009d) Paracrine signaling in a bacterium. Genes Dev 23:1631–1638PubMedPubMedCentralGoogle Scholar
  72. Mack D, Siemssen N, Laufs R (1992) Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect Immun 60:2048–2057PubMedPubMedCentralGoogle Scholar
  73. Magnuson R, Solomon J, Grossman AD (1994) Biochemical and genetic-characterization of a competence pheromone from Bacillus-subtilis. Cell 77:207–216PubMedGoogle Scholar
  74. Mavrodi DV, Blankenfeldt W, Thomashow LS (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445PubMedGoogle Scholar
  75. Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS 3rd (1992) Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 58:2616–2624PubMedPubMedCentralGoogle Scholar
  76. McDowell P, Affas Z, Reynolds C, Holden MTG, Wood SJ, Saint S, Cockayne A, Hill PJ, Dodd CER, Bycroft BW et al (2001) Structure, activity and evolution of the group I thiolactone peptide quorum-sensing system of Staphylococcus aureus. Mol Microbiol 41:503–512Google Scholar
  77. McKenney PT, Driks A, Eichenberger P (2013) The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol 11:33–44PubMedGoogle Scholar
  78. McLoon AL, Kolodkin-Gal I, Rubinstein SM, Kolter R, Losick R (2011) Spatial regulation of histidine kinases governing biofilm formation in Bacillus subtilis. J Bacteriol 193:679–685PubMedPubMedCentralGoogle Scholar
  79. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199PubMedGoogle Scholar
  80. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303–314PubMedGoogle Scholar
  81. Moker N, Dean CR, Tao J (1946–1955) Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signaling molecules. J Bacteriol(192)Google Scholar
  82. Nagorska K, Bikowski M, Obuchowski M (2007) Multicellular behaviour and production of a wide variety of toxic substances support usage of Bacillus subtilis as a powerful biocontrol agent. Acta Biochim Pol 54:495–508PubMedGoogle Scholar
  83. Ng WL, Bassler BL (2009a) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222PubMedGoogle Scholar
  84. Ng WL, Bassler BL (2009b) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222PubMedGoogle Scholar
  85. Ng WL, Perez LJ, Wei Y, Kraml C, Semmelhack MF, Bassler BL (2011) Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems. Mol Microbiol 79:1407–1417PubMedPubMedCentralGoogle Scholar
  86. Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ (2000) Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci U S A 97:10231–10235PubMedPubMedCentralGoogle Scholar
  87. Ochsner UA, Koch AK, Fiechter A, Reiser J (1994) Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol 176:2044–2054PubMedPubMedCentralGoogle Scholar
  88. Oinuma K, Greenberg EP (2011) Acyl-homoserine lactone binding to and stability of the orphan Pseudomonas aeruginosa quorum-sensing signal receptor QscR. J Bacteriol 193:421–428PubMedPubMedCentralGoogle Scholar
  89. Okegbe C, Price-Whelan A, Dietrich LE (2014) Redox-driven regulation of microbial community morphogenesis. Curr Opin Microbiol 18C:39–45Google Scholar
  90. Oppenheimer-Shaanan Y, Steinberg N, Kolodkin-Gal I (2013) Small molecules are natural triggers for the disassembly of biofilms. Trends Microbiol 21(11):594–601PubMedGoogle Scholar
  91. Perez LJ, Ng WL, Marano P, Brook K, Bassler BL, Semmelhack MF, Perez LJ, Ng WL, Marano P, Brook K, Bassler BL, Semmelhack MF (2012) Role of the CAI-1 fatty acid tail in the Vibrio cholerae quorum sensing response. J Med Chem 55(22):9669–81PubMedPubMedCentralGoogle Scholar
  92. Periasamy S, Joo HS, Duong AC, Bach TH, Tan VY, Chatterjee SS, Cheung GY, Otto M (2012) How Staphylococcus aureus biofilms develop their characteristic structure. Proc Natl Acad Sci U S A 109:1281–1286PubMedPubMedCentralGoogle Scholar
  93. Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132PubMedPubMedCentralGoogle Scholar
  94. Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH (1999a) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96:11229–11234PubMedPubMedCentralGoogle Scholar
  95. Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH (1999b) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96:11229–11234PubMedPubMedCentralGoogle Scholar
  96. Price-Whelan A, Dietrich LE, Newman DK (2006) Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78PubMedGoogle Scholar
  97. Purevdorj B, Costerton JW, Stoodley P (2002) Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 68:4457–4464PubMedPubMedCentralGoogle Scholar
  98. Ray VA, Visick KL (2012) LuxU connects quorum sensing to biofilm formation in Vibrio fischeri. Mol Microbiol 86:954–970PubMedPubMedCentralGoogle Scholar
  99. Roche FM, Meehan M, Foster TJ (2003) The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 149:2759–2767PubMedGoogle Scholar
  100. Roggiani M, Dubnau D (1993) Coma, a phosphorylated response regulator protein of Bacillus-subtilis, binds to the promoter region of Srfa. J Bacteriol 175:3182–3187PubMedPubMedCentralGoogle Scholar
  101. Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A 107:2230–2234PubMedPubMedCentralGoogle Scholar
  102. Rubinstein SM, Kolodkin-Gal I, McLoon A, Chai L, Kolter R, Losick R, Weitz DA (2012) Osmotic pressure can regulate matrix gene expression in Bacillus subtilis. Mol Microbiol 86:426–436PubMedGoogle Scholar
  103. Sadikot RT, Blackwell TS, Christman JW, Prince AS (2005) Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 171:1209–1223PubMedPubMedCentralGoogle Scholar
  104. Sanchez C (2011) Microbial ecology: bacteria reinforce plant defences. Nat Rev Microbiol 9:483PubMedGoogle Scholar
  105. Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003a) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079PubMedPubMedCentralGoogle Scholar
  106. Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003b) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079PubMedPubMedCentralGoogle Scholar
  107. Sheppard JD, Jumarie C, Cooper DG, Laprade R (1991) Ionic channels induced by surfactin in planar lipid bilayer-membranes. Biochim Biophys Acta 1064:13–23PubMedGoogle Scholar
  108. Shibata S, Yip ES, Quirke KP, Ondrey JM, Visick KL (2012) Roles of the structural symbiosis polysaccharide (syp) genes in host colonization, biofilm formation, and polysaccharide biosynthesis in Vibrio fischeri. J Bacteriol 194:6736–6747PubMedPubMedCentralGoogle Scholar
  109. Smith RS, Iglewski BH (2003) P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6:56–60PubMedGoogle Scholar
  110. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209PubMedGoogle Scholar
  111. Tegmark K, Morfeldt E, Arvidson S (1998) Regulation of agr-dependent virulence genes in Staphylococcus aureus by RNAIII from coagulase-negative staphylococci. J Bacteriol 180:3181–3186PubMedPubMedCentralGoogle Scholar
  112. Tielker D, Hacker S, Loris R, Strathmann M, Wingender J, Wilhelm S, Rosenau F, Jaeger KE (2005) Pseudomonas aeruginosa lectin LecB is located in the outer membrane and is involved in biofilm formation. Microbiology 151:1313–1323PubMedGoogle Scholar
  113. Tischler AD, Camilli A (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53:857–869PubMedPubMedCentralGoogle Scholar
  114. Tsompanidou E, Sibbald MJ, Chlebowicz MA, Dreisbach A, Back JW, van Dijl JM, Buist G, Denham EL (2011) Requirement of the agr locus for colony spreading of Staphylococcus aureus. J Bacteriol 193:1267–1272PubMedPubMedCentralGoogle Scholar
  115. Vlamakis H, Aguilar C, Losick R, Kolter R (2008) Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev 22:945–953PubMedPubMedCentralGoogle Scholar
  116. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157–168PubMedPubMedCentralGoogle Scholar
  117. Wagner-Dobler I, Thiel V, Eberl L, Allgaier M, Bodor A, Meyer S, Ebner S, Hennig A, Pukall R, Schulz S (2005) Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. Chembiochem 6:2195–2206PubMedGoogle Scholar
  118. Wang Y, Kern SE, Newman DK (2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192:365–369PubMedPubMedCentralGoogle Scholar
  119. Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, Newman DK (2011) Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J Bacteriol 193:3606–3617PubMedPubMedCentralGoogle Scholar
  120. Watnick PI, Fullner KJ, Kolter R (1999) A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol 181:3606–3609PubMedPubMedCentralGoogle Scholar
  121. Wei Y, Perez LJ, Ng WL, Semmelhack MF, Bassler BL (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 6:356–365PubMedPubMedCentralGoogle Scholar
  122. Wells IC (1952) Antibiotic substances produced by Pseudomonas aeruginosa; syntheses of Pyo Ib, Pyo Ic, and Pyo III. J Biol Chem 196:331–340PubMedGoogle Scholar
  123. Wells IC, Elliott WH, Thayer SA, Doisy EA (1952) Ozonization of some antibiotic substances produced by Pseudomonas aeruginosa. J Biol Chem 196:321–330PubMedGoogle Scholar
  124. Weng LX, Yang YX, Zhang YQ, Wang LH (2014) A new synthetic ligand that activates QscR and blocks antibiotic-tolerant biofilm formation in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 98:2565–2572PubMedGoogle Scholar
  125. Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153:1318–1328PubMedGoogle Scholar
  126. Yang L, Nilsson M, Gjermansen M, Givskov M, Tolker-Nielsen T (2009) Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol 74:1380–1392PubMedGoogle Scholar
  127. Yildiz FH, Schoolnik GK (1999) Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci U S A 96:4028–4033PubMedPubMedCentralGoogle Scholar
  128. Yildiz FH, Visick KL (2009) Vibrio biofilms: so much the same yet so different. Trends Microbiol 17:109–118PubMedPubMedCentralGoogle Scholar
  129. Yip ES, Geszvain K, DeLoney-Marino CR, Visick KL (2006) The symbiosis regulator rscS controls the syp gene locus, biofilm formation and symbiotic aggregation by Vibrio fischeri. Mol Microbiol 62:1586–1600PubMedPubMedCentralGoogle Scholar
  130. Zhu J, Mekalanos JJ (2003) Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5:647–656PubMedGoogle Scholar
  131. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 99:3129–3134PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer India 2015

Authors and Affiliations

  • Hadas Ganin
    • 1
  • Eliane Hadas Yardeni
    • 1
  • Ilana Kolodkin-Gal
    • 1
    Email author
  1. 1.Department of Molecular GeneticsWeizmann Institute of ScienceRehovotIsrael

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