Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium

Molecular Microbiology

Volumn 77, Issue 3, 2010, Pages 771-786

  Zakikhany, Katherina ^a   Harrington, Carl R ^b   Nimtz, Manfred ^c   Hinton, Jay C D ^b,d   Römling, Ute ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ADRA PROTEIN; BACTERIAL PROTEIN; CSGBA PROTEIN; CSGD PROTEIN; DEOXYRIBONUCLEASE I; HISTONE; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG; PROTEIN BINDING; TRANSACTIVATOR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; BIOFILM; CARBOXY TERMINAL SEQUENCE; DNA BINDING; DNA BINDING MOTIF; ELECTROPHORETIC MOBILITY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SALMONELLA TYPHIMURIUM; AMINO ACID SEQUENCE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SEQUENCE ALIGNMENT;

SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; TRANS-ACTIVATORS;

EID: 77954855585     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07247.x     Document Type: Article

References (96)

1. Annous, B.A., Burke, A. Sites, J.E. (2004) Surface pasteurization of whole fresh cantaloupes inoculated with Salmonella poona or Escherichia coli. J Food Prot 67 : 1876 1885.
2. Appleby, J.L. Bourret, R.B. (1999) Activation of CheY mutant D57N by phosphorylation at an alternative site, Ser-56. Mol Microbiol 34 : 915 925.
3. Austin, J.W., Sanders, G., Kay, W.W. Collinson, S.K. (1998) Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol Lett 162 : 295 301.
4. Becker, G. Hengge-Aronis, R. (2001) What makes an Escherichia coli promoter sigma(S) dependent? Role of the -13/-14 nucleotide promoter positions and region 2.5 of sigma(S). Mol Microbiol 39 : 1153 1165.
5. Birck, C., Mourey, L., Gouet, P., Fabry, B., Schumacher, J., Rousseau, P., et al. (1999) Conformational changes induced by phosphorylation of the FixJ receiver domain. Structure 7 : 1505 1515.
6. Boddicker, J.D., Ledeboer, N.A., Jagnow, J., Jones, B.D. Clegg, S. (2002) Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol Microbiol 45 : 1255 1265.
7. Bougdour, A., Lelong, C. Geiselmann, J. (2004) Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase σ subunit of RNA polymerase. J Biol Chem 279 : 19540 19550.
8. Bourret, R.B., Hess, J.F. Simon, M.I. (1990) Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc Natl Acad Sci USA 87 : 41 45.
9. Brombacher, E., Dorel, C., Zehnder, A.J. Landini, P. (2003) The curli biosynthesis regulator CsgD co-ordinates the expression of both positive and negative determinants for biofilm formation in Escherichia coli. Microbiology 149 : 2847 2857.
10. Brombacher, E., Baratto, A., Dorel, C. Landini, P. (2006) Gene expression regulation by the Curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J Bacteriol 188 : 2027 2037.
11. Casper-Lindley, C. Yildiz, F.H. (2004) VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J Bacteriol 186 : 1574 1578.
12. Cheng, H.P. Walker, G.C. (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J Bacteriol 180 : 20 26.
13. Chirwa, N.T. Herrington, M.B. (2003) CsgD, a regulator of curli and cellulose synthesis, also regulates serine hydroxymethyltransferase synthesis in Escherichia coli K-12. Microbiology 149 : 525 535.
14. Clements, M.O., Eriksson, S., Thompson, A., Lucchini, S., Hinton, J.C., Normark, S. Rhen, M. (2002) Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc Natl Acad Sci USA 99 : 8784 8789.
15. Collinson, S.K., Clouthier, S.C., Doran, J.L., Banser, P.A. Kay, W.W. (1996) Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae. J Bacteriol 178 : 662 667.
16. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16 : 10881 10890.
17. Dahl, M.K., Msadek, T., Kunst, F. Rapoport, G. (1991) Mutational analysis of the Bacillus subtilis DegU regulator and its phosphorylation by the DegS protein kinase. J Bacteriol 173 : 2539 2547.
18. Darwin, A.J., Li, J. Stewart, V. (1996) Analysis of nitrate regulatory protein NarL-binding sites in the fdnG and narG operon control regions of Escherichia coli K-12. Mol Microbiol 20 : 621 632.
19. Darwin, A.J., Tyson, K.L., Busby, S.J. Stewart, V. (1997) Differential regulation by the homologous response regulators NarL and NarP of Escherichia coli K-12 depends on DNA binding site arrangement. Mol Microbiol 25 : 583 595.
20. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
21. Dersch, P., Fsihi, H. Bremer, E. (1994) Low-copy-number T7 vectors for selective gene expression and efficient protein overproduction in Escherichia coli. FEMS Microbiol Lett 123 : 19 26.
22. Feng, X., Walthers, D., Oropeza, R. Kenney, L.J. (2004) The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol Microbiol 54 : 823 835.
23. Gao, R., Mack, T.R. Stock, A.M. (2007) Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem Sci 32 : 225 234.
24. Gerstel, U. Romling, U. (2001) Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 3 : 638 648.
25. Gerstel, U. Romling, U. (2003) The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res Microbiol 154 : 659 667.
26. Gibson, D.L., White, A.P., Snyder, S.D., Martin, S., Heiss, C., Azadi, P., et al. (2006) Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J Bacteriol 188 : 7722 7730.
27. Gruber, T.M. Gross, C.A. (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57 : 441 466.
28. Gualdi, L., Tagliabue, L. Landini, P. (2007) Biofilm formation-gene expression relay system in Escherichia coli: modulation of sigmaS-dependent gene expression by the CsgD regulatory protein via sigmaS protein stabilization. J Bacteriol 189 : 8034 8043.
29. Gueriri, I., Bay, S., Dubrac, S., Cyncynatus, C. Msadek, T. (2008) The Pta-AckA pathway controlling acetyl phosphate levels and the phosphorylation state of the DegU orphan response regulator both play a role in regulating Listeria monocytogenes motility and chemotaxis. Mol Microbiol 70 : 1342 1357.
30. Gusa, A.A., Gao, J., Stringer, V., Churchward, G. Scott, J.R. (2006) Phosphorylation of the group A Streptococcal CovR response regulator causes dimerization and promoter-specific recruitment by RNA polymerase. J Bacteriol 188 : 4620 4626.
31. Guthrie, E.P., Flaxman, C.S., White, J., Hodgson, D.A., Bibb, M.J. Chater, K.F. (1998) A response-regulator-like activator of antibiotic synthesis from Streptomyces coelicolor A3(2) with an amino-terminal domain that lacks a phosphorylation pocket. Microbiology 144 : 727 738.
32. Guvener, Z.T. McCarter, L.L. (2003) Multiple regulators control capsular polysaccharide production in Vibrio parahaemolyticus. J Bacteriol 185 : 5431 5441.
33. Hamilton, S., Bongaerts, R.J., Mulholland, F., Cochrane, B., Porter, J., Lucchini, S., et al. (2009) The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms. BMC Genomics 10 : 599.
34. Hammar, M., Arnqvist, A., Bian, Z., Olsen, A. Normark, S. (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.
35. Hoch, J.A. (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3 : 165 170.
36. Holman, T.R., Wu, Z., Wanner, B.L. Walsh, C.T. (1994) Identification of the DNA-binding site for the phosphorylated VanR protein required for vancomycin resistance in Enterococcus faecium. Biochemistry 33 : 4625 4631.
37. Hughes, T.R., Roberts, C.J., Dai, H., Jones, A.R., Meyer, M.R., Slade, D., et al. (2000) Widespread aneuploidy revealed by DNA microarray expression profiling. Nat Genet 25 : 333 337.
38. Ichikawa, J.K., Norris, A., Bangera, M.G., Geiss, G.K., van 't Wout, A.B., Bumgarner, R.E. Lory, S. (2000) Interaction of Pseudomonas aeruginosa with epithelial cells: identification of differentially regulated genes by expression microarray analysis of human cDNAs. Proc Natl Acad Sci USA 97 : 9659 9664.
39. Ishihama, A. (2000) Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54 : 499 518.
40. Jenal, U. Malone, J. (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40 : 385 407.
41. Kader, A., Simm, R., Gerstel, U., Morr, M. Romling, U. (2006) Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol Microbiol 60 : 602 616.
42. Karlinsey, J.E. (2007) lambda-Red genetic engineering in Salmonella enterica serovar Typhimurium. Methods Enzymol 421 : 199 209.
43. Klose, K.E., Weiss, D.S. Kustu, S. (1993) Glutamate at the site of phosphorylation of nitrogen-regulatory protein NTRC mimics aspartyl-phosphate and activates the protein. J Mol Biol 232 : 67 78.
44. Krasteva, P.V., Fong, J.C., Shikuma, N.J., Beyhan, S., Navarro, M.V., Yildiz, F.H. Sondermann, H. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327 : 866 868.
45. Lacour, S. Landini, P. (2004) SigmaS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of sigmaS-dependent genes and identification of their promoter sequences. J Bacteriol 186 : 7186 7195.
46. Lan, C.Y. Igo, M.M. (1998) Differential expression of the OmpF and OmpC porin proteins in Escherichia coli K-12 depends upon the level of active OmpR. J Bacteriol 180 : 171 174.
47. Latasa, C., Roux, A., Toledo-Arana, A., Ghigo, J.M., Gamazo, C., Penades, J.R. Lasa, I. (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58 : 1322 1339.
48. Lauriano, C.M., Ghosh, C., Correa, N.E. Klose, K.E. (2004) The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J Bacteriol 186 : 4864 4874.
49. Lawson, C.L., Swigon, D., Murakami, K.S., Darst, S.A., Berman, H.M. Ebright, R.H. (2004) Catabolite activator protein: DNA binding and transcription activation. Curr Opin Struct Biol 14 : 10 20.
50. Li, J., Kustu, S. Stewart, V. (1994) In vitro interaction of nitrate-responsive regulatory protein NarL with DNA target sequences in the fdnG, narG, narK and frdA operon control regions of Escherichia coli K-12. J Mol Biol 241 : 150 165.
51. Liu, W. Hulett, F.M. (1997) Bacillus subtilis PhoP binds to the phoB tandem promoter exclusively within the phosphate starvation-inducible promoter. J Bacteriol 179 : 6302 6310.
52. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 : 402 408.
53. Lukat, G.S., McCleary, W.R., Stock, A.M. Stock, J.B. (1992) Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci USA 89 : 718 722.
54. Ma, S., Selvaraj, U., Ohman, D.E., Quarless, R., Hassett, D.J. Wozniak, D.J. (1998) Phosphorylation-independent activity of the response regulators AlgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa. J Bacteriol 180 : 956 968.
55. McCleary, W.R. Stock, J.B. (1994) Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 269 : 31567 31572.
56. McCleary, W.R., Stock, J.B. Ninfa, A.J. (1993) Is acetyl phosphate a global signal in Escherichia coli? J Bacteriol 175 : 2793 2798.
57. Maris, A.E., Sawaya, M.R., Kaczor-Grzeskowiak, M., Jarvis, M.R., Bearson, S.M., Kopka, M.L., et al. (2002) Dimerization allows DNA target site recognition by the NarL response regulator. Nat Struct Biol 9 : 771 778.
58. Marschall, C., Labrousse, V., Kreimer, M., Weichart, D., Kolb, A. Hengge-Aronis, R. (1998) Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on sigma s and requires activation by cAMP-CRP. J Mol Biol 276 : 339 353.
59. Mascher, T., Helmann, J.D. Unden, G. (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70 : 910 938.
60. Moore, J.B., Shiau, S.P. Reitzer, L.J. (1993) Alterations of highly conserved residues in the regulatory domain of nitrogen regulator I (NtrC) of Escherichia coli. J Bacteriol 175 : 2692 2701.
61. Msadek, T., Kunst, F., Henner, D., Klier, A., Rapoport, G. Dedonder, R. (1990) Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol 172 : 824 834.
62. Mukai, K., Kawata, M. Tanaka, T. (1990) Isolation and phosphorylation of the Bacillus subtilis degS and degU gene products. J Biol Chem 265 : 20000 20006.
63. Munch, R., Hiller, K., Grote, A., Scheer, M., Klein, J., Schobert, M. Jahn, D. (2005) Virtual footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21 : 4187 4189.
64. Murray, E.J., Kiley, T.B. Stanley-Wall, N.R. (2009) A pivotal role for the response regulator DegU in controlling multicellular behaviour. Microbiology 155 : 1 8.
65. O'Connor, T.J. Nodwell, J.R. (2005) Pivotal roles for the receiver domain in the mechanism of action of the response regulator RamR of Streptomyces coelicolor. J Mol Biol 351 : 1030 1047.
66. Pflock, M., Bathon, M., Schar, J., Muller, S., Mollenkopf, H., Meyer, T.F. Beier, D. (2007) The orphan response regulator HP1021 of Helicobacter pylori regulates transcription of a gene cluster presumably involved in acetone metabolism. J Bacteriol 189 : 2339 2349.
67. Pruss, B.M. (1998) Acetyl phosphate and the phosphorylation of OmpR are involved in the regulation of the cell division rate in Escherichia coli. Arch Microbiol 170 : 141 146.
68. Reyrat, J.M., David, M., Batut, J. Boistard, P. (1994) FixL of Rhizobium meliloti enhances the transcriptional activity of a mutant FixJD54N protein by phosphorylation of an alternate residue. J Bacteriol 176 : 1969 1976.
69. Robbe-Saule, V., Jaumouillé, V., Prévost, M.-C., Guadagnini, S., Talhouarne, C., Mathout, H., et al. (2006) Crl activates transcription initiation of RpoS-regulated genes involved in the multicellular behavior of Salmonella enterica serovar Typhimurium. J Bacteriol 188 : 3982 3994.
70. Romling, U. (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62 : 1234 1246.
71. Romling, U. Amikam, D. (2006) Cyclic di-GMP as a second messenger. Curr Opin Microbiol 9 : 218 228.
72. Romling, U., Bian, Z., Hammar, M., Sierralta, W.D. Normark, S. (1998a) Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180 : 722 731.
73. Romling, U., Sierralta, W.D., Eriksson, K. Normark, S. (1998b) Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28 : 249 264.
74. Romling, U., Rohde, M., Olsen, A., Normark, S. Reinkoster, J. (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36 : 10 23.
75. Ross, P., Mayer, R., Weinhouse, H., Amikam, D., Huggirat, Y., Benziman, M., et al. (1990) The cyclic diguanylic acid regulatory system of cellulose synthesis in Acetobacter xylinum. Chemical synthesis and biological activity of cyclic nucleotide dimer, trimer, and phosphothioate derivatives. J Biol Chem 265 : 18933 18943.
76. Roy, C.R. Falkow, S. (1991) Identification of Bordetella pertussis regulatory sequences required for transcriptional activation of the fhaB gene and autoregulation of the bvgAS operon. J Bacteriol 173 : 2385 2392.
77. Ruiz, D., Salinas, P., Lopez-Redondo, M.L., Cayuela, M.L., Marina, A. Contreras, A. (2008) Phosphorylation-independent activation of the atypical response regulator NblR. Microbiology 154 : 3002 3015.
78. Schar, J., Sickmann, A. Beier, D. (2005) Phosphorylation-independent activity of atypical response regulators of Helicobacter pylori. J Bacteriol 187 : 3100 3109.
79. Schmittgen, T.D. Livak, K.J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3 : 1101 1108.
80. Schroder, I., Wolin, C.D., Cavicchioli, R. Gunsalus, R.P. (1994) Phosphorylation and dephosphorylation of the NarQ, NarX, and NarL proteins of the nitrate-dependent two-component regulatory system of Escherichia coli. J Bacteriol 176 : 4985 4992.
81. Simm, R., Morr, M., Kader, A., Nimtz, M. Romling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53 : 1123 1134.
82. Simm, R., Lusch, A., Kader, A., Andersson, M. Römling, U. (2007) Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J Bacteriol 189 : 3613 3623.
83. Simm, R., Morr, M., Remminghorst, U., Andersson, M. Romling, U. (2009) Quantitative determination of cyclic diguanosine monophosphate concentrations in nucleotide extracts of bacteria by matrix-assisted laser desorption/ionization- time-of-flight mass spectrometry. Anal Biochem 386 : 53 58.
84. Solano, C., Garcia, B., Valle, J., Berasain, C., Ghigo, J.M., Gamazo, C. Lasa, I. (2002) Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 43 : 793 808.
85. Stock, A.M., Robinson, V.L. Goudreau, P.N. (2000) Two-component signal transduction. Annu Rev Biochem 69 : 183 215.
86. Urbanowski, M.L., Lostroh, C.P. Greenberg, E.P. (2004) Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J Bacteriol 186 : 631 637.
87. Walker, M.S. DeMoss, J.A. (1993) Phosphorylation and dephosphorylation catalyzed in vitro by purified components of the nitrate sensing system, NarX and NarL. J Biol Chem 268 : 8391 8393.
88. Wang, L., Tian, X., Wang, J., Yang, H., Fan, K., Xu, G., et al. (2009) Autoregulation of antibiotic biosynthesis by binding of the end product to an atypical response regulator. Proc Natl Acad Sci USA 106 : 8617 8622.
89. Waters, C.M., Lu, W., Rabinowitz, J.D. Bassler, B.L. (2008) Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol 190 : 2527 2536.
90. Weinhouse, H., Sapir, S., Amikam, D., Shilo, Y., Volman, G., Ohana, P. Benziman, M. (1997) c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett 416 : 207 211.
91. Wolfe, A.J., Chang, D.E., Walker, J.D., Seitz-Partridge, J.E., Vidaurri, M.D., Lange, C.F., et al. (2003) Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol 48 : 977 988.
92. Yang, Y.H. Speed, T. (2002) Design issues for cDNA microarray experiments. Nat Rev Genet 3 : 579 588.
93. Ygberg, S.E., Clements, M.O., Rytkonen, A., Thompson, A., Holden, D.W., Hinton, J.C. Rhen, M. (2006) Polynucleotide phosphorylase negatively controls spv virulence gene expression in Salmonella enterica. Infect Immun 74 : 1243 1254.
94. Zhang, J.H., Xiao, G., Gunsalus, R.P. Hubbell, W.L. (2003) Phosphorylation triggers domain separation in the DNA binding response regulator NarL. Biochemistry 42 : 2552 2559.
95. Zhu, J. Winans, S.C. (1999) Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. Proc Natl Acad Sci USA 96 : 4832 4837.
96. Zogaj, X., Nimtz, M., Rohde, M., Bokranz, W. Romling, U. (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.