Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism

Molecular Microbiology

Volumn 76, Issue 5, 2010, Pages 1250-1265

  Dillon, Shane C ^a   Cameron, Andrew D S ^a   Hokamp, Karsten ^b   Lucchini, Sacha ^c   Hinton, Jay C D ^a   Dorman, Charles J ^a  

^a Moyne Institute of Preventive Medicine   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; PROTEIN SFH; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; AT RICH SEQUENCE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GENOME; BINDING SITE; CHROMOSOMAL LOCALIZATION; CONTROLLED STUDY; GENE REGULATORY NETWORK; GENE SILENCING; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN DNA BINDING; SALMONELLA TYPHIMURIUM;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GENE SILENCING; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; HUMANS; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; PLASMIDS; SALMONELLA TYPHIMURIUM; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; SHIGELLA FLEXNERI 2A STR. 2457T;

EID: 77952820341     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07173.x     Document Type: Article

References (82)

1. Afflerbach, H., Schröder, O. Wagner, R. (1999) Conformational changes of the upstream DNA mediated by H-NS and FIS regulate E. coli rrnB P1 promoter activity. J Mol Biol 286 : 339 353.
2. Amit, R., Oppenheim, A.B. Stavans, J. (2003) Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys J 84 : 2467 2473.
3. Amit, R., Oppenheim, A.B. Stavans, J. (2004) Single molecule elasticity measurements: a biophysical approach to bacterial nucleoid organization. Biophys J 87 : 1392 1393.
4. Bailey, T.L., Williams, N., Misleh, C. Li, W.W. (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34 : W369 W373.
5. Banos, R.C., Vivero, A., Aznar, S., Garcia, J., Pons, M., Madrid, C. Juarez, A. (2009) Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLoS Genet 5 : e1000513.
6. Beloin, C., Deighan, P., Doyle, M. Dorman, C.J. (2003) Shigella flexneri 2a strain 2457T expresses three members of the H-NS-like protein family: characterization of the Sfh protein. Mol Genet Genomics 270 : 66 77.
7. Bertin, P., Benhabiles, N., Krin, E., Laurent-Winter, C., Tendeng, C., Turlin, E., et al. (1999) The structural and functional organization of H-NS-like proteins is evolutionarily conserved in gram-negative bacteria. Mol Microbiol 31 : 319 329.
8. Beveridge, D.L., Dixit, S.B., Barreiro, G. Thayer, K.M. (2004) Molecular dynamics simulations of DNA curvature and flexibility: helix phasing and premelting. Biopolymers 73 : 380 403.
9. Bouffartigues, E., Buckle, M., Badaut, C., Travers, A. Rimsky, S. (2007) H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat Struct Mol Biol 14 : 441 448.
10. Buck, M.J., Nobel, A.B. Lieb, J.D. (2005) ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol 6 : R97.
11. Carattoli, A. (2003) Plasmid-mediated antimicrobial resistance in Salmonella enterica. Curr Issues Mol Biol 5 : 113 122.
12. Chen, C.C., Chou, M.Y., Huang, C.H., Majumder, A. Wu, H.Y. (2005) A cis-spreading nucleoprotein filament is responsible for the gene silencing activity found in the promoter relay mechanism. J Biol Chem 280 : 5101 5112.
13. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158 : 9 14.
14. Cho, B.K., Knight, E.M., Barrett, C.L. Palsson, B.O. (2008) Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res 18 : 900 910.
15. Crothers, D.M., Haran, T.E. Nadeau, J.G. (1990) Intrinsically bent DNA. J Biol Chem 265 : 7093 7096.
16. Dame, R.T., Luijsterburg, M.S., Krin, E., Bertin, P.N., Wagner, R. Wuite, G.J. (2005) DNA bridging: a property shared among H-NS-like proteins. J Bacteriol 187 : 1845 1848.
17. Dame, R.T., Noom, M.C. Wuite, G.J. (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444 : 387 390.
18. Deighan, P., Beloin, C. Dorman, C.J. (2003) Three-way interactions among the Sfh, StpA and H-NS nucleoid-structuring proteins of Shigella flexneri 2a strain 2457T. Mol Microbiol 48 : 1401 1416.
19. Deng, S., Stein, R.A. Higgins, N.P. (2005) Organization of supercoil domains and their reorganization by transcription. Mol Microbiol 57 : 1511 1521.
20. Dole, S., Nagarajavel, V. Schnetz, K. (2004) The histone-like nucleoid structuring protein H-NS represses the Escherichia coli bgl operon downstream of the promoter. Mol Microbiol 52 : 589 600.
21. Dorman, C.J. (2004) H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2 : 391 400.
22. Dorman, C.J. (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5 : 157 161.
23. Dorman, C.J. (2009) Regulatory integration of horizontally-transferred genes in bacteria. Front Biosci 14 : 4103 4112.
24. Dorman, C.J., Hinton, J.C. Free, A. (1999) Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol 7 : 124 128.
25. Doyle, M. Dorman, C.J. (2006) Reciprocal transcriptional and posttranscriptional growth-phase-dependent expression of sfh, a gene that encodes a paralogue of the nucleoid-associated protein H-NS. J Bacteriol 188 : 7581 7591.
26. Doyle, M., Fookes, M., Ivens, A., Mangan, M.W., Wain, J. Dorman, C.J. (2007) An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315 : 251 252.
27. Ellermeier, J.R. Slauch, J.M. (2007) Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol 10 : 24 29.
28. Falconi, M., McGovern, V., Gualerzi, C., Hillyard, D. Higgins, N.P. (1991) Mutations altering chromosomal protein H-NS induce mini-Mu transposition. New Biol 3 : 615 625.
29. Falconi, M., Brandi, A., La Teana, A., Gualerzi, C.O. Pon, C.L. (1996) Antagonistic involvement of FIS and H-NS proteins in the transcriptional control of hns expression. Mol Microbiol 19 : 965 975.
30. Fass, E. Groisman, E.A. (2009) Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 12 : 199 204.
31. Free, A. Dorman, C.J. (1995) Coupling of Escherichia coli hns mRNA levels to DNA synthesis by autoregulation: implications for growth phase control. Mol Microbiol 18 : 101 113.
32. Garcia-Vallve, S., Guzman, E., Montero, M.A. Romeu, A. (2003) HGT-DB: a database of putative horizontally transferred genes in prokaryotic complete genomes. Nucleic Acids Res 31 : 187 189.
33. Gitter, A., Siegfried, Z., Klutstein, M., Fornes, O., Oliva, B., Simon, I. Bar-Joseph, Z. (2009) Backup in gene regulatory networks explains differences between binding and knockout results. Mol Syst Biol 5 : 276.
34. Grainger, D.C., Overton, T.W., Reppas, N., Wade, J.T., Tamai, E., Hobman, J.L., et al. (2004) Genomic studies with Escherichia coli MelR protein: applications of chromatin immunoprecipitation and microarrays. J Bacteriol 186 : 6938 6943.
35. Grainger, D.C., Hurd, D., Harrison, M., Holdstock, J. Busby, S.J. (2005) Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 102 : 17693 17698.
36. Grainger, D.C., Hurd, D., Goldberg, M.D. Busby, S.J. (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34 : 4642 4652.
37. Grainger, D.C., Aiba, H., Hurd, D., Browning, D.F. Busby, S.J. (2007) Transcription factor distribution in Escherichia coli: studies with FNR protein. Nucleic Acids Res 35 : 269 278.
38. Haraga, A., Ohlson, M.B. Miller, S.I. (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6 : 53 66.
39. Hardy, C.D. Cozzarelli, N.R. (2005) A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol Microbiol 57 : 1636 1652.
40. Hernandez-Lucas, I., Gallego-Hernandez, A.L., Encarnacion, S., Fernandez-Mora, M., Martinez-Batallar, A.G., Salgado, H., et al. (2008) The LysR-type transcriptional regulator LeuO controls expression of several genes in Salmonella enterica serovar Typhi. J Bacteriol 190 : 1658 1670.
41. Hinton, J.C., Santos, D.S., Seirafi, A., Hulton, C.S., Pavitt, G.D. Higgins, C.F. (1992) Expression and mutational analysis of the nucleoid-associated protein H-NS of Salmonella typhimurium. Mol Microbiol 6 : 2327 2337.
42. Hokamp, K., Roche, F.M., Acab, M., Rousseau, M.E., Kuo, B., Goode, D., et al. (2004) ArrayPipe: a flexible processing pipeline for microarray data. Nucleic Acids Res 32 : W457 W459.
43. Isalan, M., Lemerle, C., Michalodimitrakis, K., Horn, C., Beltrao, P., Raineri, E., et al. (2008) Evolvability and hierarchy in rewired bacterial gene networks. Nature 452 : 840 845.
44. Jiang, X.M., Neal, B., Santiago, F., Lee, S.J., Romana, L.K. Reeves, P.R. (1991) Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar Typhimurium (strain LT2). Mol Microbiol 5 : 695 713.
45. Juhas, M., van der Meer, J.R., Gaillard, M., Harding, R.M., Hood, D.W. Crook, D.W. (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33 : 376 393.
46. Kanehisa, M., Goto, S., Hattori, M., Aoki-Kinoshita, K.F., Itoh, M., Kawashima, S., et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34 : D354 D357.
47. Koonin, E.V. Wolf, Y.I. (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36 : 6688 6719.
48. Lang, B., Blot, N., Bouffartigues, E., Buckle, M., Geertz, M., Gualerzi, C.O., et al. (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35 : 6330 6337.
49. Lee, Y.H., Kim, J.H., Bang, I.S. Park, Y.K. (2008) The membrane-bound transcriptional regulator CadC is activated by proteolytic cleavage in response to acid stress. J Bacteriol 190 : 5120 5126.
50. Liu, Y., Chen, H., Kenney, L.J. Yan, J. (2010) A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev 24 : 339 344.
51. Lucchini, S., Rowley, G., Goldberg, M.D., Hurd, D., Harrison, M. Hinton, J.C. (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2 : e81.
52. Lucchini, S., McDermott, P., Thompson, A. Hinton, J.C. (2009) The H-NS-like protein StpA represses the RpoS (sigma 38) regulon during exponential growth of Salmonella Typhimurium. Mol Microbiol 74 : 1169 1186.
53. Lucht, J.M., Dersch, P., Kempf, B. Bremer, E. (1994) Interactions of the nucleoid-associated DNA-binding protein H-NS with the regulatory region of the osmotically controlled proU operon of Escherichia coli. J Biol Chem 269 : 6578 6578.
54. MacDonald, D., Herbert, K., Zhang, X., Pologruto, T. Lu, P. (2001) Solution structure of an A-tract DNA bend. J Mol Biol 306 : 1081 1098.
55. Majdalani, N., Vanderpool, C.K. Gottesman, S. (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40 : 93 113.
56. Nagarajavel, V., Madhusudan, S., Dole, S., Rahmouni, A.R. Schnetz, K. (2007) Repression by binding of H-NS within the transcription unit. J Biol Chem 282 : 23622 23630.
57. Navarre, W.W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S.J. Fang, F.C. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313 : 236 238.
58. Navarre, W.W., McClelland, M., Libby, S.J. Fang, F.C. (2007) Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev 21 : 1456 1471.
59. Noom, M.C., Navarre, W.W., Oshima, T., Wuite, G.J. Dame, R.T. (2007) H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 17 : R913 R914.
60. Olekhnovich, I.N. Kadner, R.J. (2006) Crucial roles of both flanking sequences in silencing of the hilA promoter in Salmonella enterica. J Mol Biol 357 : 373 386.
61. Oshima, T., Ishikawa, S., Kurokawa, K., Aiba, H. Ogasawara, N. (2006) Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13 : 141 153.
62. Overdier, D.G. Csonka, L.N. (1992) A transcriptional silencer downstream of the promoter in the osmotically controlled proU operon of Salmonella typhimurium. Proc Natl Acad Sci USA 89 : 3140 3144.
63. Owen-Hughes, T.A., Pavitt, G.D., Santos, D.S., Sidebotham, J.M., Hulton, C.S., Hinton, J.C. Higgins, C.F. (1992) The chromatin-associated protein H-NS interacts with curved DNA to influence DNA topology and gene expression. Cell 71 : 255 265.
64. Pearson, W.R. (1991) Searching protein sequence libraries: comparison of the sensitivity and selectivity of the Smith-Waterman and FASTA algorithms. Genomics 11 : 635 650.
65. Pedersen, A.G., Jensen, L.J., Brunak, S., Staerfeldt, H.H. Ussery, D.W. (2000) A DNA structural atlas for Escherichia coli. J Mol Biol 299 : 907 930.
66. Ponty, Y., Termier, M. Denise, A. (2006) GenRGenS: software for generating random genomic sequences and structures. Bioinformatics 22 : 1534 1535.
67. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A. Barrell, B. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16 : 944 945.
68. Schnetz, K. (1995) Silencing of Escherichia coli bgl promoter by flanking sequence elements. EMBO J 14 : 2545 2550.
69. Schröder, O. Wagner, R. (2000) The bacterial DNA-binding protein H-NS represses ribosomal RNA transcription by trapping RNA polymerase in the initiation complex. J Mol Biol 298 : 737 748.
70. Sette, M., Spurio, R., Trotta, E., Brandizi, C., Brandi, A., Pon, C.L., et al. (2009) Sequence-specific recognition of DNA by the C-terminal domain of nucleoid-associated protein H-NS. J Biol Chem 284 : 30453 30462.
71. Shimada, T., Ishihama, A., Busby, S.J. Grainger, D.C. (2008) The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res 36 : 3950 3955.
72. Smyth, G.K. Speed, T. (2003) Normalization of cDNA microarray data. Methods 31 : 265 273.
73. Stoebel, D.M., Free, A. Dorman, C.J. (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154 : 2533 2545.
74. Stormo, G.D. Hartzell, G.W., 3rd. (1989) Identifying protein-binding sites from unaligned DNA fragments. Proc Natl Acad Sci USA 86 : 1183 1187.
75. Tendeng, C. Bertin, P.N. (2003) H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol 11 : 511 518.
76. Thomas-Chollier, M., Sand, O., Turatsinze, J.V., Janky, R., Defrance, M., Vervisch, E., et al. (2008) RSAT: regulatory sequence analysis tools. Nucleic Acids Res 36 : W119 W127.
77. Ueguchi, C., Seto, C., Suzuki, T. Mizuno, T. (1997) Clarification of the dimerization domain and its functional significance for the Escherichia coli nucleoid protein H-NS. J Mol Biol 274 : 145 151.
78. Uzzau, S., Figueroa-Bossi, N., Rubino, S. Bossi, L. (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA 98 : 15264 15269.
79. Vora, T., Hottes, A.K. Tavazoie, S. (2009) Protein occupancy landscape of a bacterial genome. Mol Cell 35 : 247 253.
80. Wain, J., Diem Nga, L.T., Kidgell, C., James, K., Fortune, S., Song Diep, T., et al. (2003) Molecular analysis of IncHI1 antimicrobial resistance plasmids from Salmonella serovar Typhi strains associated with typhoid fever. Antimicrob Agents Chemother 47 : 2732 2739.
81. Walthers, D., Carroll, R.K., Navarre, W.W., Libby, S.J., Fang, F.C. Kenney, L.J. (2007) The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS. Mol Microbiol 65 : 477 493.
82. Wei, J., Goldberg, M.B., Burland, V., Venkatesan, M.M., Deng, W., Fournier, G., et al. (2003) Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect Immun 71 : 2775 2786.