Biofilms: Maintenance, development, and disassembly of bacterial communities are determined by QS cascades

Quorum Sensing vs Quorum Quenching: A Battle with no end in Sight

Volumn , Issue , 2015, Pages 23-37

  Ganin, Hadas ^a   Yardeni, Eliane Hadas ^a   Kolodkin Gal, Ilana ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BACTERIOLOGY;

BACILLUS SUBTILIS; BACTERIAL COMMUNITY; CHEMICAL COMMUNICATIONS; FILAMENTOUS CELLS; MULTICELLULAR COMMUNITIES; MULTICELLULAR STRUCTURE; SPORE FORMATION; UNICELLULAR ORGANISMS;

BIOFILMS;

EID: 84943383661     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-81-322-1982-8__3     Document Type: Chapter

References (131)

1. Aguilar C, Vlamakis H, Losick R, Kolter R (2007) Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10:638–643
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 59:1114–1128
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 31:488–494
4. Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102:11076–11081
5. Baron SS, Rowe JJ (1981) Antibiotic action of pyocyanin. Antimicrob Agents Chemother 20:814–820
6. Bassler BL, Losick R (2006) Bacterially speaking. Cell 125:237–246
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:E1621–1630
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 151:373–383
9. Boles BR, Horswill AR (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052
10. Boles BR, Horswill AR (2011) Staphylococcal biofilm disassembly. Trends Microbiol 19:449–455
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 98:11621–11626
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 186:3970–3979
13. Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229–1238
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 90:2187–2196
15. Bryers JD (2008) Medical biofilms. Biotechnol Bioeng 100:1–18
16. Cha M, Hong S, Kang MY, Lee JW, Jang J (2012) Gasphase removal of biofilms from various surfaces using carbon dioxide aerosols. Biofouling 28:681–686
17. Chai Y, Chu F, Kolter R, Losick R (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67:254–263
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 85:418–430
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 15:848–864
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 215:41–46
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 41:435–464
22. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322
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 12:102
24. Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036
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 280:295–298
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 67:1865–1873
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: 998–1014
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 61:1308–1321
29. Dietrich LE, Teal TK, Price-Whelan A, Newman DK (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203–1206
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 195:1371–1380
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 50:29–43
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 8:1095–1104
33. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449
34. Ellermeier CD, Hobbs EC, Gonzalez-Pastor JE, Losick R (2006) A three-protein signaling pathway governing immunity to a bacterial cannibalism toxin. Cell 124:549–559
35. Engebrecht J, Nealson K, Silverman M (1983) Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32:773–781
36. Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2:e135
37. Faruque SM, Albert MJ, Mekalanos JJ (1998) Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62:1301
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-Nacetylglucosamine. Int Forum Allergy Rhinol 3:83–88
39. Fujita M, Gonzalez-Pastor JE, Losick R (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187:1357–1368
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 92:399–412
41. Gonzalez-Pastor JE, Hobbs EC, Losick R (2003) Cannibalism by sporulating bacteria. Science 301:510–513
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 byPseudomonas aeruginosa isolates from cystic fibrosis airways. Proc Natl Acad Sci U S A 100:2771–2776
43. Ha C, Park SJ, Im SJ, Park SJ, Lee JH (2012) Interspecies signaling through QscR, a quorum receptor of Pseudomonas aeruginosa. Mol Cells 33:53–59
44. Hammer BK, Bassler BL (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50:101–104
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 159:725–750
46. Henke JM, Bassler BL (2004) Three parallel quorumsensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186:6902–6914
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 148:87–102
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 22:3803–3815
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 22:3803–3815
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 450:883
51. Kearns DB, Chu F, Branda SS, Kolter R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55:739–749
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 quorumsensing autoinducer CAI-1: analysis of the biosynthetic enzyme CqsA. Nat Chem Biol 5:891–895
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 111:208–213
54. Kirisits MJ, Parsek MR (2006) Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities? Cell Microbiol 8:1841–1849
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 231:107–110
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 151:3589–3602
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 27:887–899
58. Kolter R, Greenberg EP (2006) Microbial sciences: the superficial life of microbes. Nature 441:300–302
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 21:1137–1146
60. Lau GW, Hassett DJ, Ran H, Kong F (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10:599–606
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 48:199–210
62. Lee SH, Hava DL, Waldor MK, Camilli A (1999) Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99:625–634
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 1622:36–41
64. Lequette Y, Greenberg EP (2005) Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37–44
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 188:3365–3370
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 108:15763–15768
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 188:4442–4452
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 106:280–285
69. Lopez D, Vlamakis H, Kolter R (2009b) Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33:152–163
70. Lopez D, Vlamakis H, Losick R, Kolter R (2009c) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74:609–618
71. Lopez D, Vlamakis H, Losick R, Kolter R (2009d) Paracrine signaling in a bacterium. Genes Dev 23:1631–1638
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 60:2048–2057
73. Magnuson R, Solomon J, Grossman AD (1994) Biochemical and genetic-characterization of a competence pheromone from Bacillus-subtilis. Cell 77:207–216
74. Mavrodi DV, Blankenfeldt W, Thomashow LS (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445
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 58:2616–2624
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 quorumsensing system of Staphylococcus aureus. Mol Microbiol 41:503–512
77. McKenney PT, Driks A, Eichenberger P (2013) The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol 11:33–44
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 193:679–685
79. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199
80. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303–314
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)
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: 495–508
83. Ng WL, Bassler BL (2009a) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222
84. Ng WL, Bassler BL (2009b) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222
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 79:1407–1417
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 97:10231–10235
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 176:2044–2054
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 193:421–428
89. Okegbe C, Price-Whelan A, Dietrich LE (2014) Redoxdriven regulation of microbial community morphogenesis. Curr Opin Microbiol 18C:39–45
90. Oppenheimer-Shaanan Y, Steinberg N, Kolodkin-Gal I (2013) Small molecules are natural triggers for the disassembly of biofilms. Trends Microbiol 21(11): 594–601
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):9669–81
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 109:1281–1286
93. Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132
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 96:11229–11234
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 96:11229–11234
96. Price-Whelan A, Dietrich LE, Newman DK (2006) Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78
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 68:4457–4464
98. Ray VA, Visick KL (2012) LuxU connects quorum sensing to biofilm formation in Vibrio fischeri. Mol Microbiol 86:954–970
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 149:2759–2767
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: 3182–3187
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 107:2230–2234
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 86:426–436
103. Sadikot RT, Blackwell TS, Christman JW, Prince AS (2005) Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 171:1209–1223
104. Sanchez C (2011) Microbial ecology: bacteria reinforce plant defences. Nat Rev Microbiol 9:483
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 185:2066–2079
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 185:2066–2079
107. Sheppard JD, Jumarie C, Cooper DG, Laprade R (1991) Ionic channels induced by surfactin in planar lipid bilayer-membranes. Biochim Biophys Acta 1064:13–23
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 194:6736–6747
109. Smith RS, Iglewski BH (2003) P. aeruginosa quorumsensing systems and virulence. Curr Opin Microbiol 6:56–60
110. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209
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 180:3181–3186
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 151:1313–1323
113. Tischler AD, Camilli A (2004) Cyclic diguanylate (cdi-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53:857–869
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 193:1267–1272
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 22:945–953
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: 157–168
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 longchain quorum sensing signals in free-living and hostassociated marine alphaproteobacteria. Chembiochem 6:2195–2206
118. Wang Y, Kern SE, Newman DK (2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192:365–369
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 193:3606–3617
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: 3606–3609
121. Wei Y, Perez LJ, Ng WL, Semmelhack MF, Bassler BL (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 6:356–365
122. Wells IC (1952) Antibiotic substances produced by Pseudomonas aeruginosa; syntheses of Pyo Ib, Pyo Ic, and Pyo III. J Biol Chem 196:331–340
123. Wells IC, Elliott WH, Thayer SA, Doisy EA (1952) Ozonization of some antibiotic substances produced by Pseudomonas aeruginosa. J Biol Chem 196:321–330
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: 2565–2572
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 153:1318–1328
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 74:1380–1392
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 96:4028–4033
128. Yildiz FH, Visick KL (2009) Vibrio biofilms: so much the same yet so different. Trends Microbiol 17:109–118
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 62:1586–1600
130. Zhu J, Mekalanos JJ (2003) Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5:647–656
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 99:3129–3134