Chapter 4 : Molecular Basis of Biofilm Development by Pseudomonads

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Molecular Basis of Biofilm Development by Pseudomonads, Page 1 of 2

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Many of the tools for studying biofilms were developed in pseudomonads and, as such, these organisms have become a key model system for biofilm development by gram-negative bacteria. This chapter discusses what is known about biofilm development in pseudomonads and present working models of biofilm formation by these organisms. Cells are released from mature biofilms and reenter the planktonic state, making biofilm development a cyclic pathway in pseudomonads. Inorganic phosphate may be a key environmental factor required for biofilm formation by pseudomonads. and mutants lacking flagella have colonization defects on biotic surfaces, such as plant seeds and roots, and abiotic surfaces, such as sand, soil, plastic, and silicone. In , a complex between the virulence factor regulator (Vfr) and cAMP will form under glucose-limiting conditions. The study of the mechanisms of biofilm maintenance will likely be a fruitful area of investigation in the coming years. The chapter reviews what little is known about maintaining mature biofilm structure. A biofilm acts as reservoir for bacterial expansion in which successful colonization in one location subsequently permits surface exploration of numerous regions. The chapter discusses what is known about the biology of bacterial detachment. Insight into the biology of detachment will be a useful tool in the design of therapeutic agents for the fight against biofilm-based infections and for the disinfection of surfaces found in clinical and industrial settings.

Citation: Toutain C, Caiazza N, O’Toole G. 2004. Molecular Basis of Biofilm Development by Pseudomonads, p 43-63. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch4
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Model of biofilm development by pseudomonads. Planktonic cells (step 1) attach to the surface (step 2) first reversibly, then irreversibly, and start to develop microcolonies (step 3) either by aggregation of already attached cells, by recruitment of planktonic cells, or by clonal growth. These microcolonies then proliferate and mature (step 4) into a “mushroom shape” or a “carpet-like” biofilm, depending on environmental conditions and strain. Images were obtained during flow cell experiments by phase-contrast microscopy from a top-down view (magnification of ×630).

Citation: Toutain C, Caiazza N, O’Toole G. 2004. Molecular Basis of Biofilm Development by Pseudomonads, p 43-63. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch4
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1. Albus, A. M.,, E. C. Pesci,, L. J. Runyen- Janecky,, S. E. West,, and B. H. Iglewski. 1997. Vfr controls quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179:39283935.
2. Allison, D. G.,, B. Ruiz,, C. SanJose,, A. Jaspe,, and P. Gilbert. 1998. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol. Lett. 167:179184.
3. Al-Tahhan, R. A.,, T. R. Sandrin,, A. A. Bodour,, and R. M. Maier. 2000. Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl. Environ. Microbiol. 66:32623268.
4. Beatson, S. A.,, C. B. Whitchurch,, J. L. Sargent,, R. C. Levesque,, and J. S. Mattick. 2002a. Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J. Bacteriol. 184:36053613.
5. Beatson, S. A.,, C. B. Whitchurch,, A. B. Semmler,, and J. S. Mattick. 2002b. Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J. Bacteriol. 184:35983604.
6. Boyd, A.,, and A. M. Chakrabarty. 1994. Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 60:23552359.
7. Bruinsma, G. M.,, M. Rustema-Abbing,, J. de Vries,, H. J. Busscher,, M. L. van der Linden,, J. M. Hooymans,, and H. C. van der Mei. 2003. Multiple surface properties of worn RGP lenses and adhesion of Pseudomonas aeruginosa. Biomaterials 24:16631670.
8. Bruinsma, G. M.,, H. C. van der Mei,, and H. J. Busscher. 2001. Bacterial adhesion to surface hydrophilic and hydrophobic contact lenses. Biomaterials 22:32173224.
9. Busalmen, J. P.,, and S. R. de Sanchez. 2001. Influence of pH and ionic strength on adhesion of a wild strain of Pseudomonas sp. to titanium. J. Ind. Microbiol. Biotechnol. 26:303308.
10. Casaz, P.,, A. Happel,, J. Keithan,, D. L. Read,, S. R. Strain,, and S. B. Levy. 2001. The Pseudomonas fluorescens transcription activator AdnA is required for adhesion and motility. Microbiology 147:355361.
11. Chancey, S. T.,, D. W. Wood,, and L. S. Pierson III. 1999. Two-component transcriptional regulation of N-acyl-homoserine lactone production in Pseudomonas aureofaciens. Appl. Environ. Microbiol. 65:22942299.
12. Characklis, W. G.,, G. A. McFeters,, and K. C. Marshall,. 1990. Physiological ecology in biofilm systems, p. 341394. In W. G. Characklis, and K. C. Marshall (ed.), Biofilms. John Wiley & Sons, Inc., New York, N.Y.
13. Chiang, P.,, and L. L. Burrows. 2003. Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J. Bacteriol. 185:23742378.
14. Costerton, J. W.,, Z. Lewandowski,, D. E. Caldwell,, D. R. Korber,, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711745.
15. Davey, M. E.,, N. C. Caiazza,, and G. A. O’Toole. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185:10271036.
16. Davey, M. E.,, and G. O. O’Toole. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847867.
17. DeFlaun, M. F.,, B. M. Marshall,, E.-P. Kulle,, and S. B. Levy. 1994. Tn5 insertion mutants of Pseudomonas fluorescens defective in adhesion to soil and seeds. Appl. Environ. Microbiol. 60:26372642.
18. DeFlaun, M. F.,, S. R. Oppenheimer,, S. Streger,, C. W. Condee,, and M. Fletcher. 1999. Alterations in adhesion, transport, and membrane characteristics in an adhesion-deficient pseudomonad. Appl. Environ. Microbiol. 65:759765.
19. DeFlaun, M. F.,, A. S. Tanzer,, A. L. McAteer,, B. Marshall,, and S. B. Levy. 1990. Development of an adhesion assay and characterization of an adhesion-deficient mutant of Pseudomonas fluorescens. Appl. Environ. Microbiol. 56:112119.
20. De Kievit, T. R.,, R. Gillis,, S. Marx,, C. Brown,, and B. H. Iglewski. 2001. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67:18651873.
21. Dekkers, L. C.,, A. J. van der Bij,, I. H. M. Mulders,, C. C. Phoelich,, R. A. R. Wentwoord,, D. C. M. Glandorf,, C. A. Wijffelman,, and B. J. J. Lugtenberg. 1998. Role of the O-antigen of lipopolysaccharide, and possible roles of growth rate and of NADH:ubiquinone oxidoreductase (nuo) in competitive tomato root-tip colonization by Pseudomonas fluorescens WCS365. Mol. Plant-Microbe Interact. 11:763771.
22. Delaquis, P. J.,, D. E. Caldwell,, J. R. Lawrence,, and A. R. McCurdy. 1989. Detachment of Pseudomonas fluorescens from biofilms on glass surfaces in response to nutrient stress. Microb. Ecol. 18:199210.
23. de Weert, S.,, H. Vermeiren,, I. H. Mulders,, I. Kuiper,, N. Hendrickx,, G. V. Bloemberg,, J. Van der leyden,, R. De Mot,, and B. J. Lugtenberg. 2002. Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol. Plant-Microbe Interact. 15:11731180.
24. De Weger, L.,, M. C. M. van Loosdrecht,, H. E. Klaassen,, and B. Lugtenberg. 1989. Mutational changes in physiochemical cell surface properties of plant-growth-stimulating Pseudomonas spp. do not influence the attachment properties of cells. J. Bacteriol. 171:27562761.
25. De Weger, L. A.,, C. I. M. van der Vlught,, A. H. M. Wijfjes,, P. A. H. M. Bakker,, B. Schippers,, and B. Lugtenberg. 1987. Flagella of a plant-growth-stimulating Pseudomonas fluorescens are required for colonization of potato roots. J. Bacteriol. 169:27692773.
26. Deziel, E.,, Y. Comeau,, and R. Villemur. 2001. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J. Bacteriol. 183:11951204.
27. Drenkard, E.,, and F. M. Ausubel. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740743.
28. Dussart, L.,, J. P. Dupont,, I. Zimmerlin,, M. Lacroix,, J. M. Saiter,, G. A. Junter,, and T. Jouenne. 2003. Occurrence of sessile Pseudomonas oryzihabitans from a karstified chalk aquifer. Water Res. 37:15931600.
29. Dybvig, K. 1993. DNA rearrangements and phenotypic switching in prokaryotes. Mol. Microbiol. 10:465471.
30. Espinosa-Urgel, M.,, A. Salido,, and J. L. Ramos. 2000. Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J. Bacteriol. 182:23632369.
31. Finelli, A.,, C. V. Gallant,, K. Jarvi,, and L. L. Burrows. 2003. Use of in-biofilm expression technology to identify genes involved in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185:27002710.
32. Fletcher, M. 1988. Attachment of Pseudomonas fluorescens to glass and influence of electrolytes on bacterium-substratum separation distance. J. Bacteriol. 170:20272030.
33. Fujita, M.,, K. Tanaka,, H. Takahashi,, and A. Amemura. 1994. Transcription of the principal sigma-factor genes, rpoD and rpoS, in Pseudomonas aeruginosa is controlled according to the growth phase. Mol. Microbiol. 13:10711077.
34. Gacesa, P.,, R. C. Caswell,, and P. Kille. 1989. Bacterial alginases. Antibiot. Chemother. 42:6771.
35. Gallagher, L. A.,, S. L. McKnight,, M. S. Kuznetsova,, E. C. Pesci,, and C. Manoil. 2002. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J. Bacteriol. 184:64726480.
36. Gallegos, M. T.,, R. Schleif,, A. Bairoch,, K. Hofmann,, and J. L. Ramos. 1997. Arac/XylS family of transcriptional regulators. Microbiol. Mol. Biol. Rev. 61:393410.
37. Gomez-Suarez, C.,, H. J. Busscher,, and H. C. van der Mei. 2001. Analysis of bacterial detachment from substratum surfaces by the passage of air-liquid interfaces. Appl. Environ. Microbiol. 67:25312537.
38. Grewal, S. I.,, B. Han,, and K. Johnstone. 1995. Identification and characterization of a locus which regulates multiple functions in Pseudomonas tolaasii, the cause of brown blotch disease of Agaricus bisporus. J. Bacteriol. 177:46584668.
39. Haussler, S.,, B. Tummler,, H. Weissbrodt,, M. Rohde,, and I. Steinmetz. 1999. Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin. Infect. Dis. 29:621625.
40. Haussler, S.,, I. Ziegler,, A. Lottel,, F. von Gotz,, M. Rohde,, D. Wehmhohner,, S. Saravanamuthu,, B. Tummler,, and I. Steinmetz. 2003. Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J. Med. Microbiol. 52:295301.
41. Henderson, I. R.,, P. Owen,, and J. P. Nataro. 1999. Molecular switches: the ON and OFF of bacterial phase variation. Mol. Microbiol. 33:919932.
42. Henrichsen, J. 1975. The occurrence of twitching motility among gram-negative bacteria. Acta Pathol. Microbiol. Scand. Sect. B 83:171178.
43. Henrichsen, J. 1983. Twitching motility. Annu. Rev. Microbiol. 37:8193.
44. Henrici, A. T. 1933. Studies of freshwater bacteria. I. A direct microscopic technique. J. Bacteriol. 25:277287.
45. Hentzer, M.,, G. M. Teitzel,, G. J. Balzer,, A. Heydorn,, S. Molin,, M. Givskov,, and M. R. Parsek. 2001. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183:53955401.
46. Heydorn, A.,, B. Ersboll,, J. Kato,, M. Hentzer,, M. R. Parsek,, T. Tolker-Nielsen,, M. Givskov,, and S. Molin. 2002. 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. 68:20082017.
47. Hinsa, S. M.,, M. Espinosa-Urgel,, J. L. Ramos,, and G. A. O’Toole. 2003. Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol. Microbiol. 49:905918.
48. Hogan, D. A.,, and R. Kolter. 2002. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296:22292232.
49. Horn, H.,, H. Reiff,, and E. Morgenroth. 2003. Simulation of growth and detachment in biofilm systems under defined hydrodynamic conditions. Biotechnol. Bioeng. 81:607617.
50. Jana, T. K.,, A. K. Srivastava,, K. Csery,, and D. K. Arora. 2000. Influence of growth and environmental conditions on cell surface hydrophobicity of Pseudomonas fluorescens in non-specific adhesion. Can. J. Microbiol. 46:2837.
51. Jorgensen, F.,, M. Bally,, V. Chapon-Herve,, G. Michel,, A. Lazdunski,, P. Williams,, and G. S. Stewart. 1999. RpoS-dependent stress tolerance in Pseudomonas aeruginosa. Microbiology 145:835844.
52. Kadurugamuwa, J. L.,, and T. J. Beveridge. 1995. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J. Bacteriol. 177:39984008.
53. Klausen, M.,, A. Heydorn,, P. Ragas,, L. Lambertsen,, A. Aaes-Jorgensen,, S. Molin,, and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48:15111524.
54. Koenig, D. W.,, S. K. Mishra,, and D. L. Pierson. 1995. Removal of Burkholderia cepacia biofilms with oxidants. Biofouling 9:5162.
55. Laville, J.,, C. Voisard,, C. Keel,, M. Maurhofer,, G. DeFago,, and D. Hass. 1992. Global control in Pseudomonas fluorescens mediating antibiotic synthesis and supression of black root rot of tobacco. Proc. Natl. Acad. Sci. USA 89:15621566.
56. Lawrence, J. R.,, P. J. Delaquis,, D. R. Korber,, and D. E. Caldwell. 1987. Behavior of Pseudomonas fluorescens within the hydrodynamic boundary layers of surface microenvironments. Microb. Ecol. 14:114.
57. Liao, C. H.,, D. Mc Callus,, and W. Fett. 1994. Molecular characterization of two gene loci required for production of the key pathogenicity factor pectate lyase in Pseudomonas viridiflava. Mol. Plant-Microbe Interact. 7:391400.
58. Loewen, P. C.,, B. Hu,, J. Strutinsky,, and R. Sparling. 1998. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 44:707717.
59. MacGregor, C. H.,, S. K. Arora,, P. W. Hager,, M. B. Dail, , and P. V. Phibbs, Jr. 1996. The nucleotide sequence of the Pseudomonas aeruginosa pyrE-crc-rph region and the purification of the crc gene product. J. Bacteriol. 178:56275635.
60. Makin, S. A.,, and T. J. Beveridge. 1996. The influence of A-band and B-band lipopolysaccharide on the surface characteristics and adhesion of Pseudomonas aeruginosa to surfaces. Microbiology 142:299307.
61. Marshall, K. C.,, R. Stout,, and R. Mitchell. 1971. Mechanism of the initial events in the sorbtion of marine bacteria to surfaces. J. Gen. Microbiol. 68:337348.
62. Marshall, P. A.,, G. I. Loeb,, M. M. Cowan,, and M. Fletcher. 1989. Response of microbial adhesives and biofilm matrix polymers to chemical treatments as determined by interference relection microscopy and light selection microscopy. Appl. Environ. Microbiol. 55:28272831.
63. McEldowney, S. 1994. Effect of cadmium and zinc on attachment and detachment interactions of Pseudomonas fluorescens H2 with glass. Appl. Environ. Microbiol. 60:27592765.
64. Merz, A. J.,, M. So,, and M. P. Sheetz. 2000. Pilus retraction powers bacterial twitching motility. Nature 407:98102.
65. Miller, M. J.,, and D. G. Ahearn. 1987. Adherence of Pseudomonas aeruginosa to hydrophilic contact lenses and other substrata. J. Clin. Microbiol. 25:13921397.
66. Monds, R. D.,, M. W. Silby,, and H. K. Mahanty. 2001. Expression of the Pho regulon negatively regulates biofilm formation by Pseudomonas aureofaciens PA147-2. Mol. Microbiol. 42:415426.
67. Moreno, M.,, J. P. Audia,, S. M. Bearson,, C. Webb,, and J. W. Foster. 2000. Regulation of sigma S degradation in Salmonella enterica var Typhimurium: in vivo interactions between sigma S, the response regulator MviA(RssB) and ClpX. J. Mol. Microbiol. Biotechnol. 2:245254.
68. Morett, E.,, and L. Segovia. 1993. The sigma 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains. J. Bacteriol. 175:60676074.
69. Mulligan, C. N.,, G. Mahmourides,, and B. F. Gibbs. 1989. The influence of phosphate metabolism on biosurfactant production by Pseudomonas aeruginosa. J. Biotechnol. 12:199210.
70. Murga, R.,, J. M. Miller,, and R. M. Donlan, 2001. Biofilm formation by gram-negative bacteria on central venous catheter connectors: effect of conditioning films in a laboratory model. J. Clin. Microbiol. 39:22942297.
71. Muto, Y.,, and S. Goto. 1986. Transformation by extracellular DNA produced by Pseudomonas aeruginosa. Microbiol. Immunol. 30:621628.
72. Neu, T. R. 1996. Signifigance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol. Rev. 60:151166.
73. Nickel, J. C.,, I. Ruseska,, J. B. Wright,, and J. W. Costerton. 1985. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary tract catheter. Antimicrob. Agents Chemother. 27:619624.
74. Ochsner, U. A.,, A. K. Koch,, A. Fiechter,, and J. Reiser. 1994. Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J. Bacteriol. 176:20442054.
75. Ochsner, U. A.,, and J. Reiser. 1995. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92:64246428.
76. Ohashi, A.,, and H. Harada. 1996. A novel concept for evaluation of biofilm adhesion strength by applying tensile force and shear force. Water Sci. Technol. 34:201211.
77. Ohashi, A.,, T. Koyama,, K. Syutsubo,, and H. Harada. 1999. A novel method for evaluation of biofilm tensile strength resisting erosion. Water Sci. Technol. 39:261268.
78. O’Toole, G. A.,, K. A. Gibbs,, P. W. Hager, , P. V. Phibbs, Jr.,, and R. Kolter. 2000. The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 182:425431.
79. O’Toole, G. A.,, and R. Kolter. 1998a. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295304.
80. O’Toole, G. A.,, and R. Kolter. 1998b. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449461.
81. Ott, C. M.,, D. F. Day,, D. W. Koenig,, and D. L. Pierson. 2001. The release of alginate lyase from growing Pseudomonas syringae pathovar phaseolicola. Curr. Microbiol. 42:7881.
82. Parkins, M. D.,, H. Ceri,, and D. G. Storey. 2001. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol. Microbiol. 40:12151226.
83. Pesci, E. C.,, J. P. Pearson,, P. C. Seed,, and B. H. Iglewski. 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179:31273132.
84. Picioreanu, C.,, M. C. Van Loosdrecht,, and J. J. Heijnen. 2000a. Effect of diffusive and convective substrate transport on biofilm structure formation: a two-dimensional modeling study. Biotechnol. Bioeng. 69:504515.
85. Picioreanu, C.,, M. C. van Loosdrecht,, and J. J. Heijnen. 2000b. A theoretical study on the effect of surface roughness on mass transport and transformation in biofilms. Biotechnol. Bioeng. 68:355369.
86. Picioreanu, C.,, M. C. van Loosdrecht,, and J. J. Heijnen. 2001. Two-dimensional model of biofilm detachment caused by internal stress from liquid flow. Biotechnol. Bioeng. 72:205218.
87. Piette, J. P.,, and E. S. Idziak. 1991. Role of flagella in adhesion of Pseudomonas fluorescens to tendon slices. Appl. Environ. Microbiol. 57:16351639.
88. Pratt, L. A.,, and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30:285294.
89. Prince, A. 1992. Adhesins and receptors of Pseudomonas aeruginosa associated with infection of the respiratory tract. Microb. Pathog. 13:251260.
90. Pringle, J. H.,, and M. Fletcher. 1986. Influence of substratum hydration and adsorbed macromolecules on bacterial attachment to surfaces. Appl. Environ. Microbiol. 51:13211325.
91. Pringle, J. H.,, M. Fletcher,, and D. C. Ellwood. 1983. Selection of attachment mutants during the continous culture of Pseudomonas fluorescens and relationship between attachment ability and surface composition. J. Gen. Microbiol. 129:25572569.
92. Rashid, M. H.,, and A. Kornberg. 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 97:48854890.
93. Rashid, M. H.,, K. Rumbaugh,, L. Passador,, D. G. Davies,, A. N. Hamood,, B. H. Iglewski,, and A. Kornberg. 2000. Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 97:96369641.
94. Rasmussen, K.,, and K. Ostgaard. 2003. Adhesion of the marine bacterium Pseudomonas sp. NCIMB 2021 to different hydrogel surfaces. Water Res. 37:519524.
95. Reimmann, C.,, M. Beyeler,, A. Latifi,, H. Winteler,, M. Foglino,, A. Lazdunski,, and D. Hass. 1997. The global activator GacA of Pseudomonas aeruginosa PAO1 positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol. Microbiol. 24:309319.
96. Rich, J. J.,, T. G. Kinscherf,, T. Kitten,, and D. K. Willis. 1994. Genetic evidence that the gacA gene encodes the cognate response regulator for the lemA sensor in Pseudomonas syringae. J. Bacteriol. 176:74687475.
97. Robleto, E. A.,, I. Lopez-Hernandez,, M. W. Silby,, and S. B. Levy. 2003. Genetic analysis of the AdnA regulon in Pseudomonas fluorescens: nonessential role of flagella in adhesion to sand and biofilm formation. J. Bacteriol. 185:453460.
98. Ron, E. Z.,, and E. Rosenberg. 2001. Natural roles of biosurfactants. Environ. Microbiol. 3:229236.
99. Sanchez-Contreras, M.,, M. Martin,, M. Villacieros,, F. O’Gara,, I. Bonilla,, and R. Rivilla, 2002. Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J. Bacteriol. 184:15871596.
100. Sauer, K.,, and A. K. Camper. 2001. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J. Bacteriol. 183:65796589.
101. Sauer, K.,, A. K. Camper,, G. D. Ehrlich,, J. W. Costerton,, and D. G. Davies. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184:11401154.
102. Simpson, D. A.,, R. Ramphal,, and S. Lory. 1995. Characterization of Pseudomonas aeruginosa fliO, a gene involved in flagellar biosynthesis and adherence. Infect. Immun. 63:29502957.
103. Singh, P. K.,, M. R. Parsek,, E. P. Greenberg,, and M. J. Welsh. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417:552555.
104. Skerker, J. M.,, and H. C. Berg. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA 98:69016904.
105. Slusher, M. M.,, Q. N. Myrvik,, J. C. Lewis,, and A. G. Gristina. 1987. Extended-wear lenses, biofilm, and bacterial adhesion. Arch. Ophthalmol. 105:110115.
106. Stewart, P. S.,, G. A. McFeters,, and C. T. Huang,. 2000. Biofilm formation and persistence, p. 373405. In J. D. Bryers (ed.), Biofilms II: Process Analysis and Application. Wiley-Liss, New York, N.Y.
107. Stoodley, P.,, R. Cargo,, C. J. Rupp,, S. Wilson,, and I. Klapper. 2002. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J. Ind. Microbiol. Biotechnol. 29:361367.
108. Stoodley, P.,, D. deBeer,, and H. M. Lappin-Scott. 1997. Influence of electric fields and pH on biofilm structure as related to the bioelectric effect. Antimicrob. Agents Chemother. 41:18761879.
109. Stoodley, P.,, Z. Lewandowski,, J. D. Boyle,, and H. M. Lappin-Scott. 1999. Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology. Biotechnol. Bioeng. 65:8392.
110. Tanaka, K.,, and H. Takahashi. 1994. Cloning, analysis and expression of an rpoS homologue from Pseudomonas aeruginosa PAO1. Gene 150:8185.
111. Taylor, G. T.,, D. Zheng,, M. Lee,, P. J. Troy,, G. Gyananath,, and S. K. Sharma. 1997. Influence of surface properties on accumulation of conditioning films and marine bacteria on substrata exposed to oligotrophic waters. Biofouling 11:3157.
112. Thanassi, D. G.,, and S. J. Hultgren. 2000. Assembly of complex organelles: pilus biogenesis in gram-negative bacteria as a model system. Methods 20:111126.
113. Tolaas, A. G. 1915. A bacterial disease of cultivated mushrooms. Phytopathology 5:5154.
114. Tolker-Nielsen, T.,, U. C. Brinch,, P. C. Ragas,, J. B. Andersen,, C. S. Jacobsen,, and S. Molin. 2000. Development and dynamics of Pseudomonas sp. biofilms. J. Bacteriol. 182:64826489.
115. Vallet, I.,, J. W. Olson,, S. Lory,, A. Lazdunski,, and A. Filloux. 2001. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc. Natl. Acad. Sci. USA 98:69116916.
116. Vesper, S. J. 1987. Production of pili (fimbriae) by Pseudomonas fluorescens and correlation with attachment to corn roots. Appl. Environ. Microbiol. 53:13971405.
117. Whitchurch, C. B.,, R. A. Alm,, and J. S. Mattick. 1996. The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 93:98399843.
118. Whitchurch, C. B.,, T. Tolker-Nielsen,, P. C. Ragas,, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487.
119. Whiteley, M.,, M. G. Bangera,, R. E. Bumgarner,, M. R. Parsek,, G. M. Teitzel,, S. Lory,, and E. P. Greenberg. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860864.
120. Whiteley, M.,, M. R. Parsek,, and E. P. Greenberg. 2000. Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J. Bacteriol. 182:43564360.
121. Williams, V.,, and M. Fletcher. 1996. Pseudomonas fluorescens adhesion and transport through porous media are affected by lipopolysaccharide composition. Appl. Environ. Microbiol. 62:100104.
122. Willis, D. K.,, J. J. Holmstadt,, and T. G. Kinscherf. 2001. Genetic evidence that loss of virulence associated with gacS or gacA mutations in Pseudomonas syringae B728a does not result from effects on alginate production. Appl. Environ. Microbiol. 67:14001403.
123. Wimpenny, J. W. T.,, and R. Colasanti. 1997. A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models. FEMS Microbiol. Ecol. 22:116.
124. Wolff, J. A.,, C. H. MacGregor,, R. C. Eisenberg, , and P. V. Phibbs, Jr. 1991. Isolation and characterization of catabolite repression control mutants of Pseudomonas aeruginosa PAO1. J. Bacteriol. 173:47004706.
125. Wong, S. M.,, P. A. Carroll,, L. G. Rahme,, F. M. Ausubel,, and S. B. Calderwood. 1998. Modulation of expression of the ToxR regulon in Vibrio cholerae by a member of the two-component family of response regulators. Infect. Immun. 66:58545861.
126. Wrangstadh, M.,, P. L. Conway,, and S. Kjelleberg. 1989. The role of an extracellular polysaccharide produced by the marine Pseudomonas sp. S9 in cellular detachment during starvation. Can. J. Microbiol. 35:309312.
127. Xu, K. D.,, M. J. Franklin,, C. H. Park,, G. A. McFeters,, and P. S. Stewart. 2001. Gene expression and protein levels of the stationary phase sigma factor, RpoS, in continuously-fed Pseudomonas aeruginosa biofilms. FEMS Microbiol. Lett. 199:6771.
128. Zobell, C. E. 1943. The effects of solid surfaces upon bacterial activity. J. Bacteriol. 46:3956.
129. Zoutman, D. E.,, W. C. Hulbert,, B. L. Pasloske,, A. M. Joffe,, K. Volpel,, M. K. Trebilcock,, and W. Paranchych. 1991. The role of polar pili in the adherence of Pseudomonas aeruginosa to injured canine tracheal cells: a semiquantitative morphologic study. Scanning Microsc. 5:109126.


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Summary of factors involved in biofilm development

Citation: Toutain C, Caiazza N, O’Toole G. 2004. Molecular Basis of Biofilm Development by Pseudomonads, p 43-63. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch4

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