A novel two-component system BqsS-BqsR modulates quorum sensing-dependent biofilm decay in Pseudomonas aeruginosa

References

• Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol 1995; 49:711 - 745
   PubMed Web of Science ®Google Scholar
• Quinn JP. Pseudomonas aeruginosa infections in the intensive care unit. Semin Respir Crit Care Med 2003; 24:61 - 68
   PubMed Web of Science ®Google Scholar
• Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999; 284:1318 - 1322
   PubMed Web of Science ®Google Scholar
• O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000; 54:49 - 79
   PubMed Web of Science ®Google Scholar
• Stoodley P, Cargo R, Rupp CJ, Wilson S, Klapper I. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J Ind Microbiol Biotechnol 2002; 29:361 - 367
   PubMed Web of Science ®Google Scholar
• Klausen M, Gjermansen M, Kreft JU, Tolker-Nielsen T. Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol Lett 2006; 261:1 - 11
   PubMed Web of Science ®Google Scholar
• Schooling SR, Charaf UK, Allison DG, Gilbert P. A role for rhamnolipid in biofilm dispersion. Biofilms 2004; 1:91 - 99
   Google Scholar
• Boles BR, Thoendel M, Singh PK. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 2005; 57:1210 - 1223
   PubMed Web of Science ®Google Scholar
• Bollinger N, Hassett DJ, Iglewski BH, Costerton JW, McDermott TR. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J Bacteriol 2001; 183:1990 - 1996
   PubMed Web of Science ®Google Scholar
• Hunt SM, Werner EM, Huang B, Hamilton MA, Stewart PS. Hypothesis for the role of nutrient starvation in biofilm detachment. Appl Environ Microbiol 2004; 70:7418 - 7425
   PubMed Web of Science ®Google Scholar
• Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P. Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 2004; 186:7312 - 7326
   PubMed Web of Science ®Google Scholar
• Singh PK, Parsek MR, Greenberg EP, Welsh MJ. A component of innate immunity prevents bacterial biofilm development. Nature 2002; 417:552 - 555
   PubMed Web of Science ®Google Scholar
• Allison DG, Ruiz B, SanJose C, Jaspe A, Gilbert P. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol Lett 1998; 167:179 - 184
   PubMed Web of Science ®Google Scholar
• Boyd A, Chakrabarty AM. Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl Environ Microbiol 1994; 60:2355 - 2359
   PubMed Web of Science ®Google Scholar
• Pamp SJ, Tolker-Nielsen T. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 2007; 189:2531 - 2539
   PubMed Web of Science ®Google Scholar
• Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998; 280:295 - 298
   PubMed Web of Science ®Google Scholar
• Heydorn A, Ersbøll B, Kato J, Hentzer M, Parsek MR, Tolker-Nielsen T, Givskov M, Molin S. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Appl Environ Microbiol 2002; 68:2008 - 2017
   PubMed Web of Science ®Google Scholar
• Ochsner UA, Fiechter A, Reiser J. Isolation, characterization and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J Biol Chem 1994; 269:19787 - 19795
   PubMed Web of Science ®Google Scholar
• Sperandio V, Torres AG, Kaper JB. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 2002; 43:809 - 821
   PubMed Web of Science ®Google Scholar
• Deziel E, Lepine F, Milot S, Villemur R. rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 2003; 149:2005 - 2013
   PubMed Web of Science ®Google Scholar
• Kohler T, Curty LK, Barja F, van Delden C, Pechere JC. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 2000; 182:5990 - 5996
   PubMed Web of Science ®Google Scholar
• Ochsner UA, Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1995; 92:6424 - 6428
   PubMed Web of Science ®Google Scholar
• Pearson JP, Pesci EC, Iglewski BH. Roles of Pseudomonas aeruginosa las and rhl quorumsensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 1997; 179:5756 - 5767
   PubMed Web of Science ®Google Scholar
• Rahim R, Ochsner UA, Olvera C, Graninger M, Messner P, Lam JS, Soberon-Chavez G. Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol Microbiol 2001; 40:708 - 718
   PubMed Web of Science ®Google Scholar
• McKnight SL, Iglewski BH, Pesci EC. The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 2000; 182:2702 - 2708
   PubMed Web of Science ®Google Scholar
• Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1999; 96:11229 - 11234
   PubMed Web of Science ®Google Scholar
• Baysse C, Cullinane M, Denervaud V, Burrowes E, Dow JM, Morrissey JP, Tam L, Trevors JT, O'Gara F. Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology 2005; 151:2529 - 2542
   Google Scholar
• Bredenbruch F, Nimtz M, Wray V, Morr M, Muller R, Haussler S. Biosynthetic pathway of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines. J Bacteriol 2005; 187:3630 - 3635
   PubMed Web of Science ®Google Scholar
• Diggle SP, Cornelis P, Williams P, Camara M. 4-quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 2006; 296:83 - 91
   PubMed Web of Science ®Google Scholar
• Diggle SP, Winzer K, Chhabra SR, Worrall KE, Camara M, Williams P. 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 2003; 50:29 - 43
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R, Ishihama A. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 2005; 280:1448 - 1456
   PubMed Web of Science ®Google Scholar
• Rodrigue A, Quentin Y, Lazdunski A, Mejean V, Foglino M. Two-component systems in Pseudomonas aeruginosa: why so many?. Trends Microbiol 2000; 8:498 - 504
   PubMed Web of Science ®Google Scholar
• Reimmann C, Beyeler M, Latifi A, Winteler H, Foglino M, Lazdunski A, Haas D. The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide and lipase. Mol Microbiol 1997; 24:309 - 319
   PubMed Web of Science ®Google Scholar
• Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, Lory S. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 2004; 7:745 - 754
   PubMed Web of Science ®Google Scholar
• Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C, Molin S, Bleves S, Lazdunski A, Lory S, Filloux A. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 2006; 103:171 - 176
   PubMed Web of Science ®Google Scholar
• Dubuis C, Rolli J, Lutz M, Defago G, Haas D. Thiamine-auxotrophic mutants of Pseudomonas fluorescens CHA0 are defective in cell-cell signaling and biocontrol factor expression. Appl Environ Microbiol 2006; 72:2606 - 2613
   PubMed Web of Science ®Google Scholar
• Kay E, Humair B, Denervaud V, Riedel K, Spahr S, Eberl L, Valverde C, Haas D. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 2006; 188:6026 - 6033
   PubMed Web of Science ®Google Scholar
• Parkins MD, Ceri H, Storey DG. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 2001; 40:1215 - 1226
   PubMed Web of Science ®Google Scholar
• Choi KS, Veeraragouda Y, Cho KM, Lee SO, Jo GR, Cho K, Lee K. Effect of gacS and gacA mutations on colony architecture, surface motility, biofilm formation and chemical toxicity in Pseudomonas sp. KL28. J Microbiol 2007; 45:492 - 498
   PubMed Web of Science ®Google Scholar
• Yang S, Peng Q, Zhang Q, Yi X, Choi CJ, Reedy RM, Charkowski AO, Yang CH. Dynamic regulation of GacA in type III secretion, pectinase gene expression, pellicle formation and pathogenicity of Dickeya dadantii (Erwinia chrysanthemi 3937). Mol Plant Microbe Interact 2008; 21:133 - 142
   PubMed Web of Science ®Google Scholar
• Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 2002; 184:6472 - 6480
   PubMed Web of Science ®Google Scholar
• Rashid MH, Kornberg A. Inorganic polyphosphate is needed for swimming, swarming and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2000; 97:4885 - 4890
   PubMed Web of Science ®Google Scholar
• Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 1998; 212:77 - 86
   PubMed Web of Science ®Google Scholar
• Heeb S, Itoh Y, Nishijyo T, Schnider U, Keel C, Wade J, Walsh U, O'Gara F, Haas D. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-associated bacteria. Mol Plant Microbe Interact 2000; 13:232 - 237
   PubMed Web of Science ®Google Scholar
• Sambrook JF, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual 1989; Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press
   Google Scholar
• O'Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 1998; 30:295 - 304
   PubMed Web of Science ®Google Scholar
• King EO, Ward MK, Raney DE. Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 1954; 44:301 - 307
   PubMed Web of Science ®Google Scholar
• Dong YH, Xu JL, Li XZ, Zhang LH. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 2000; 97:3526 - 3531
   PubMed Web of Science ®Google Scholar
• McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GS, Williams P. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 1997; 143:3703 - 3711
   PubMed Web of Science ®Google Scholar
• Zhang HB, Wang LH, Zhang LH. Coico R, Stevenson JQ B. Detection and analysis of quorum-quenching enzymes against acyl homoserine lactone qurom-sensing signals. Current Protocols in Microbiol 2007; John Wiley and Sons, Inc.
   Google Scholar
• Simon R, Priefer U, Puhler A. A broad range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/Technol 1983; 1:784 - 791
   Web of Science ®Google Scholar