Tight modulation of Escherichia coli bacterial biofilm formation through controlled expression of adhesion factors

Applied and Environmental Microbiology

Volumn 73, Issue 10, 2007, Pages 3391-3403

  Da Re, Sandra ^a   Le Quéré, Benjamin ^a   Ghigo, Jean Marc ^a   Beloin, Christophe ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; BACTERIA; BIOREMEDIATION; ESCHERICHIA COLI; GENE EXPRESSION; SANITATION;

GENETIC AMENABILITY; INDUSTRIAL ENVIRONMENT; PATHOGEN DEVELOPMENT;

BIOFILMS;

ADHESIN; CELL ADHESION MOLECULE; CELLULOSE;

ADHESION; BACTERIUM; BIOFILM; BIOREMEDIATION; BIOTECHNOLOGY; GENETICS; PATHOGEN;

ARTICLE; BIOFILM; BIOREMEDIATION; BIOTECHNOLOGY; CONTROLLED STUDY; ESCHERICHIA COLI; GENE CASSETTE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE OVEREXPRESSION; GENETIC COMPLEMENTATION; GENETIC MANIPULATION; NONHUMAN; OPERON;

ADHESINS, ESCHERICHIA COLI; BACTERIAL ADHESION; BETA-GALACTOSIDASE; BIOFILMS; CELLULASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; OPERON; PROMOTER REGIONS (GENETICS); RECOMBINATION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 34249683768     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02625-06     Document Type: Article

References (86)

1. Aouad, G., J. L. Crovisier, V. A. Geoffroy, J. M. Meyer, and P. Stille. 2006. Microbially-mediated glass dissolution and sorption of metals by Pseudomonas aeruginosa cells and biofilm. J. Hazard. Mater. 136:889-895.
2. Beech, I. B., J. A. Sunner, and K. Hiraoka. 2005. Microbe-surface interactions in biofouling and biocorrosion processes. Int. Microbiol. 8:157-168.
3. Beloin, C., S. Da Re, and J.-M. Ghigo. August 2005, posting date. Chapter 8.3.1.3, Colonization of abiotic surfaces. In R. Curtiss III, A. Böck, J. L. Ingraham, J. B. Kaper, F. C. Neidhardt, M. Riley, and C. L. Squires (ed.), EcoSal - Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC. http://www.ecosal.org.
4. Beloin, C., K. Michaelis, K. Lindner, P. Landini, J. Hacker, J.-M. Ghigo, and U. Dobrindt. 2006. The transcriptional antiterminator RfaH represses biofilm formation in Escherichia coli. J. Bacteriol. 188:1316-1331.
5. Beloin, C., J. Valle, P. Latour-Lambert, P. Faure, M. Kzreminski, D. Balestrino, J. A. Haagensen, S. Molin, G. Prensier, B. Arbeille, and J.-M. Ghigo. 2004. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51:659-674.
6. Bokranz, W., X. Wang, H. Tschape, and U. Romling. 2005. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J. Med. Microbiol. 54:1171-1182.
7. Branda, S. S., S. Vik, L. Friedman, and R. Kolter. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13:20-26.
8. Chalova, V., C. L. Woodward, and S. C. Ricke. 2006. Application of an Escherichia coli green fluorescent protein-based lysine biosensor under non-sterile conditions and autofluorescence background. Lett. Appl. Microbiol. 42:265-270.
9. Chaveroche, M. K., J.-M. Ghigo, and C. d'Enfert. 2000. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res. 28:E97.
10. Coetser, S. E., and T. E. Cloete. 2005. Biofouling and biocorrosion in industrial water systems. Crit. Rev. Microbiol. 31:213-232.
11. Cookson, A. L., W. A. Cooley, and M. J. Woodward. 2002. The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int. J. Med. Microbiol. 292:195-205.
12. Costerton, J. W., L. Montanaro, and C. R. Arciola. 2005. Biofilm in implant infections: its production and regulation. Int. J. Artif. Organs 28:1062-1068.
13. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
14. Crespo, J. G., S. Velizarov, and M. A. Reis. 2004. Membrane bioreactors for the removal of anionic micropollutants from drinking water. Curr. Opin. Biotechnol. 15:463-468.
15. Cursino, L., D. Smajs, J. Smarda, R. M. Nardi, J. R. Nicoli, E. Chartone-Souza, and A. M. Nascimento. 2006. Exoproducts of the Escherichia coli strain H22 inhibiting some enteric pathogens both in vitro and in vivo. J. Appl. Microbiol. 100:821-829.
16. Danese, P. N., L. A. Pratt, S. L. Dove, and R. Kolter. 2000. The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol. Microbiol. 37:424-432.
17. Danese, P. N., L. A. Pratt, and R. Kolter. 2000. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182:3593-3596.
18. Da Re, S., and J.-M. Ghigo. 2006. A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J. Bacteriol. 188:3073-3087.
19. Darouiche, R. O., J. I. Thornby, C. Cerra-Stewart, W. H. Donovan, and R. A. Hull. 2005. Bacterial interference for prevention of urinary tract infection: a prospective, randomized, placebo-controlled, double-blind pilot trial. Clin. Infect. Dis. 41:1531-1534.
20. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
21. Derbise, A., B. Lesic, D. Dacheux, J.-M. Ghigo, and E. Carniel. 2003. A rapid and simple method for inactivating chromosomal genes in Yersinia. FEMS Immunol. Med. Microbiol. 1590:1-4.
22. Diaz, E., A. Ferrandez, M. A. Prieto, and J. L. Garcia. 2001. Biodegradation of aromatic compounds by Escherichia coli. Microbiol. Mol. Biol Rev. 65: 523-569.
23. Diderichsen, B. 1980. flu, a metastable gene controlling surface properties of Escherichia coli. J. Bacteriol. 141:858-867.
24. Duncker, S. C., A. Lorentz, B. Schroeder, G. Breves, and S. C. Bischoff. 2006. Effect of orally administered probiotic E. coli strain Nissle 1917 on intestinal mucosal immune cells of healthy young pigs. Vet. Immunol. Immunopathol. 111:239-250.
25. Ehrt, S., X. V. Guo, C. M. Hickey, M. Ryou, M. Monteleone, L. W. Riley, and D. Schnappinger. 2005. Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res. 33:e21.
26. Erable, B., I. Goubet, S. Lamare, M. D. Legoy, and T. Maugard. 2006. Bioremediation of halogenated compounds: comparison of dehalogenating bacteria and improvement of catalyst stability. Chemosphere 65:1146-1152.
27. Focareta, A., J. C. Paton, R. Morona, J. Cook, and A. W. Paton. 2006. A recombinant probiotic for treatment and prevention of cholera. Gastroenterology 130:1688-1695.
28. Fric, P., and M. Zavoral. 2003. The effect of non-pathogenic Escherichia coli in symptomatic uncomplicated diverticular disease of the colon. Eur. J. Gastroenterol. Hepatol. 15:313-315.
29. Geissendorfer, M., and W. Hillen. 1990. Regulated expression of heterologous genes in Bacillus subtilis using the Tn10 encoded tet regulatory elements. Appl. Microbiol. Biotechnol. 33:657-663.
30. Ghigo, J.-M. 2001. Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442-445.
31. Grabig, A., D. Paclik, C. Guzy, A. Dankof, D. C. Baumgart, J. Erckenbrecht, B. Raupach, U. Sonnenborn, J. Eckert, R. R. Schumann, B. Wiedenmann, A. U. Dignass, and A. Sturm. 2006. Escherichia coli strain Nissle 1917 ameliorates experimental colitis via Toll-like receptor 2- and Toll-like receptor 4-dependent pathways. Infect. Immun. 74:4075-4082.
32. Hammar, M., A. Arnqvist, Z. Bian, A. Olsen, and S. Normark. 1995. Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol. Microbiol. 18:661-670.
33. Hejnova, J., U. Dobrindt, R. Nemcova, C. Rusniok, A. Bomba, L. Frangeul, J. Hacker, P. Glaser, P. Sebo, and C. Buchrieser. 2005. Characterization of the flexible genome complement of the commensal Escherichia coli strain A0 34/86 (083 : K24 : H31). Microbiology 151:385-398.
34. Henderson, I. R., M. Meehan, and P. Owen. 1997. A novel regulatory mechanism for a novel phase-variable outer membrane protein of Escherichia coli. Adv. Exp. Med. Biol. 412:349-355.
35. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
36. Henderson, I. R., F. Navarro-Garcia, and J. P. Nataro. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:370-378.
37. Henker, J., F. Schuster, and K. Nissler. 2001. Successful treatment of gut-caused halitosis with a suspension of living non-pathogenic Escherichia coli bacteria: a case report. Eur. J. Pediatr. 160:592-594.
38. Hillen, W., and C. Berens. 1994. Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Annu. Rev. Microbiol. 48:345-369.
39. Hoffman, L. R., D. A. D'Argenio, M. J. MacCoss, Z. Zhang, R. A. Jones, and S. I. Miller. 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171-1175.
40. Jeong, Y., B. G. Park, and J. S. Chung. 2005. High performance biofilm process for treating wastewater discharged from coal refining plants containing nitrogen, cyanide and thiocyanate. Water Sci. Technol. 52:325-334.
41. Ji, Y., B. Zhang, S. F. Van Horn, P. Warren, G. Woodnutt, M. K. Burnham, and M. Rosenberg. 2001. Identification of critical staphylococcal genes using conditional phenotypes generated by antisense RNA. Science 293:2266-2269.
42. Karthikeyan, S., and T. J. Beveridge. 2002. Pseudomonas aeruginosa biofilms react with and precipitate toxic soluble gold. Environ. Microbiol. 4:667-675.
43. Kierek-Pearson, K., and E. Karatan. 2005. Biofilm development in bacteria. Adv. Appl. Microbiol. 57:79-111.
44. Kjaergaard, K., M. A. Schembri, C. Ramos, S. Molin, and P. Klemm. 2000. Antigen 43 facilitates formation of multispecies biofilms. Environ. Microbiol. 2:695-702.
45. Klemm, P., R. M. Vejborg, and O. Sherlock. 2006. Self-associating autotransporters, SAATs: functional and structural similarities. Int. J. Med. Microbiol. 296:187-195.
46. Lehner, A., K. Riedel, L. Eberl, P. Breeuwer, B. Diep, and R. Stephan. 2005. Biofilm formation, extracellular polysaccharide production, and cell-to-cell signaling in various Enterobacter sakazakii strains: aspects promoting environmental persistence. J. Food Prot. 68:2287-2294.
47. Lesic, B., S. Bach, J.-M. Ghigo, U. Dobrindt, J. Hacker, and E. Carniel. 2004. Excision of the high-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor. Mol. Microbiol. 52:1337-1348.
48. Lindsay, D., and A. von Holy. 13 October 2006. Bacterial biofilms within the clinical setting: what healthcare professionals should know. J. Hosp. Infect. 64:313-325. doi:10.1016/j.jhin.2006.06.028. [Epub ahead of print.]
49. Lutz, R., and H. Bujard. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/ I1-I2 regulatory elements. Nucleic Acids Res. 25:1203-1210.
50. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Morgan-Kiss, R. M., C. Wadler, and J. E. Cronan, Jr. 2002. Long-term and homogeneous regulation of the Escherichia coli araBAD promoter by use of a lactose transporter of relaxed specificity. Proc. Natl. Acad. Sci. USA 99: 7373-7377.
52. Morikawa, M. 2006. Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J. Biosci. Bioeng. 101:1-8.
53. Norman, A., L. H. Hansen, and S. J. Sorensen. 2006. A flow cytometry-optimized assay using an SOS-green fluorescent protein (SOS-GFP) whole-cell biosensor for the detection of genotoxins in complex environments. Mutat. Res. 603:164-172.
54. O'Connell, H. A., C. Niu, and E. S. Gilbert. 20 October 2006. Enhanced high copy number plasmid maintenance and heterologous protein production in an Escherichia coli biofilm. Biotechnol. Bioeng. doi:10.1002/bit.21240. [Epub ahead of print.]
55. Oliva, B., G. Gordon, P. McNicholas, G. Ellestad, and I. Chopra. 1992. Evidence that tetracycline analogs whose primary target is not the bacterial ribosome cause lysis of Escherichia coli. Antimicrob. Agents Chemother. 36:913-919.
56. Oomen, C. J., P. van Ulsen, P. van Gelder, M. Feijen, J. Tommassen, and P. Gros. 2004. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23:1257-1266.
57. Owen, P. 1983. Antigens of the Escherichia coli cell envelope, p. 347-373. In O. J. Bjerrum (ed.), Electroimmunochemical analysis of membrane proteins. Elsevier Science Publishing, Amsterdam, The Netherlands.
58. Owen, P., M. Meehan, H. de Loughry-Doherty, and I. Henderson. 1996. Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol. Med. Microbiol. 16:63-76.
59. 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. 30:285-293.
60. Prigent-Combaret, C., G. Prensier, T. T. Le Thi, O. Vidal, P. Lejeune, and C. Dorel. 2000. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ. Microbiol. 2:450-464.
61. Qian, F., and W. Pan. 2002. Construction of a tetR- integrated Salmonella enterica serovar Typhi CVD908 strain that tightly controls expression of the major merozoite surface protein of Plasmodium falciparum for applications in human vaccine production. Infect. Immun. 70:2029-2038.
62. Ramey, B. E., M. Koutsoudis, S. B. von Bodman, and C. Fuqua. 2004. Biofilm formation in plant-microbe associations. Curr. Opin. Microbiol. 7:602-609.
63. Reisner, A., J. A. Haagensen, M. A. Schembri, E. L. Zechner, and S. Molin. 2003. Development and maturation of Escherichia coli K-12 biofilms. Mol. Microbiol. 48:933-946.
64. Rembacken, B. J., A. M. Snelling, P. M. Hawkey, D. M. Chalmers, and A. T. Axon. 1999. Non-pathogenic Escherichia coli versus mesalazinc for the treatment of ulcerative colitis: a randomised trial. Lancet 354:635-639.
65. Rizk, S. S., M. J. Cuneo, and H. W. Hellinga. 2006. Identification of cognate ligands for the Escherichia coli phnD protein product and engineering of a reagentless fluorescent biosensor for phosphonates. Protein Sci. 15:1745-1751.
66. Roche, A., J. McFadden, and P. Owen. 2001. Antigen 43, the major phase-variable protein of the Escherichia coli outer membrane, can exist as a family of proteins encoded by multiple alleles. Microbiology 147:161-169.
67. Romling, U. 2005. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life Sci. 62:1234-1246.
68. Roux, A., C. Beloin, and J.-M. Ghigo. 2005. Combined inactivation and expression strategy to study gene function under physiological conditions: application to identification of new Escherichia coli adhesins. J. Bacteriol. 187:1001-1013.
69. Sailer, F. C., B. M. Meberg, and K. D. Young. 2003. Beta-lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol. Lett. 226:245-249.
70. Schmidt, F. R. 2004. Recombinant expression systems in the pharmaceutical industry. Appl. Microbiol. Biotechnol. 65:363-372.
71. Shiloach, J., and R. Fass. 2005. Growing E. coli to high cell density: historical perspective on method development. Biotechnol. Adv. 23:345-357.
72. Shinkyo, R., M. Kamakura, S. Ikushiro, K. Inouye, and T. Sakaki. 2006. Biodegradation of dioxins by recombinant Escherichia coli expressing rat CYP1A1 or its mutant. Appl. Microbiol. Biotechnol. 72:584-590.
73. Singh, R., D. Paul, and R. K. Jain. 2006. Biofilms: implications in bioremediation. Trends Microbiol. 14:389-397.
74. Skiadas, I. V., H. N. Gavala, J. E. Schmidt, and B. K. Ahring. 2003. Anaerobic granular sludge and biofilm reactors. Adv. Biochem. Eng. Biotechnol. 82:35-67.
75. Stoodley, P., K. Sauer, D. G. Davies, and J. W. Costerton. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56:187-209.
76. Sung, B. H., C. H. Lee, B. J. Yu, J. H. Lee, J. Y. Lee, M. S. Kim, F. R. Blattner, and S. C. Kim. 2006. Development of a biofilm production-deficient Escherichia coli strain as a host for biotechnological applications. Appl. Environ. Microbiol. 72:3336-3342.
77. Trautner, B. W., R. A. Hull, and R. O. Darouiche. 2003. Escherichia coli 83972 inhibits catheter adherence by a broad spectrum of uropathogens. Urology 61:1059-1062.
78. Ulett, G. C., J. Valle, C. Beloin, O. Sherlock, J.-M. Ghigo, and M. A. Schembri. Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect. Immun., in press.
79. Van Houdt, R., and C. W. Michiels. 2005. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res. Microbiol. 156:626-633.
80. Vidal, O., R. Longin, C. Prigent-Combaret, C. Dorel, M. Hooreman, and P. Lejeune. 1998. Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J. Bacteriol. 180:2442-2449.
81. Viggiani, A., G. Olivieri, L. Siani, A. Di Donato, A. Marzocchella, P. Salatino, P. Barbieri, and E. Galli. 2006. An airlift biofilm reactor for the biodegradation of phenol by Pseudomonas stutzeri OX1. J. Biotechnol. 123: 46-1-477.
82. Waldron, D. E., P. Owen, and C. J. Dorman. 2002. Competitive interaction of the OxyR DNA-binding protein and the Dam methylase at the antigen 43 gene regulatory region in Escherichia coli. Mol. Microbiol. 44:509-520.
83. Wallecha, A., V. Munster, J. Correnti, T. Chan, and M. van der Woude. 2002. Dam- and OxyR-dependcnt phase variation of agn43: essential elements and evidence for a new role of DNA methylation. J. Bacteriol. 184:3338-3347.
84. Wang, X., J. F. Preston III, and T. Romeo. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 186:2724-2734.
85. Webb, J. S., M. Givskov, and S. Kjelleberg. 2003. Bacterial biofilms: prokaryotic adventures in multicellularity. Curr. Opin. Microbiol. 6:578-585.
86. Zogaj, X., M. Nimtz, M. Rohde, W. Bokranz, and U. Romling. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39:1452-1463.