The identification of response regulator-specific binding sites reveals new roles of two-component systems in Bacillus cereus and closely related low-GC Gram-positives

Environmental Microbiology

Volumn 10, Issue 10, 2008, Pages 2796-2809

  De Been, Mark ^a,b,c   Bart, Marieke J ^b   Abee, Tjakko ^a,c   Siezen, Roland J ^a,b,d   Francke, Christof ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d NIZO FOOD RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; TRANSCRIPTION FACTOR;

ADAPTATION; ARTICLE; BACILLUS CEREUS; BINDING SITE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE REPEAT; OPERATOR GENE; REGULON; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; BACILLUS CEREUS; BINDING SITES; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; OPERATOR REGIONS (GENETICS); REGULON; REPETITIVE SEQUENCES, NUCLEIC ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

BACILLUS CEREUS; BACILLUS CEREUS GROUP; BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 51649111882     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2008.01700.x     Document Type: Article

References (78)

1. Abee, T. Wouters, J.A. (1999) Microbial stress response in minimal processing. Int J Food Microbiol 50 : 65 91.
2. Aguilar, P.S., Hernandez-Arriaga, A.M., Cybulski, L.E., Erazo, A.C. de Mendoza, D. (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20 : 1681 1691.
3. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. Lipman, D.J. (1997) Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25 : 3389 3402.
4. Asai, K., Baik, S.H., Kasahara, Y., Moriya, S. Ogasawara, N. (2000) Regulation of the transport system for C4-dicarboxylic acids in Bacillus subtilis. Microbiology 146 (Part 2 263 271.
5. Baikalov, I., Schröder, I., Kaczor-Grzeskowiak, M., Grzeskowiak, K., Gunsalus, R.P. Dickerson, R.E. (1996) Structure of the Escherichia coli response regulator NarL. Biochemistry 35 : 11053 11061.
6. Bailey, T.L. Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2 : 28 36.
7. Bailey, T.L. Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14 : 48 54.
8. Bateman, A., Coin, L., Durbin, R., Finn, R.D., Hollich, V., Griffiths-Jones, S., et al. (2004) The Pfam protein families database. Nucleic Acids Res 32 : D138 D141.
9. de Been, M., Francke, C., Moezelaar, R., Abee, T. Siezen, R.J. (2006) Comparative analysis of two-component signal transduction systems of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis. Microbiology 152 : 3035 3048.
10. Bijlsma, J.J. Groisman, E.A. (2003) Making informed decisions: regulatory interactions between two-component systems. Trends Microbiol 11 : 359 366.
11. Blanco, A.G., Sola, M., Gomis-Rüth, F.X. Coll, M. (2002) Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 10 : 701 713.
12. Brunsing, R.L., La Clair, C., Tang, S., Chiang, C., Hancock, L.E., Perego, M. Hoch, J.A. (2005) Characterization of sporulation histidine kinases of Bacillus anthracis. J Bacteriol 187 : 6972 6981.
13. Crooks, G.E., Hon, G., Chandonia, J.M. Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res 14 : 1188 1190.
14. Cybulski, L.E., del Solar, G., Craig, P.O., Espinosa, M. de Mendoza, D. (2004) Bacillus subtilis DesR functions as a phosphorylation-activated switch to control membrane lipid fluidity. J Biol Chem 279 : 39340 39347.
15. Dandekar, T., Snel, B., Huynen, M. Bork, P. (1998) Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem Sci 23 : 324 328.
16. Duport, C., Zigha, A., Rosenfeld, E. Schmitt, P. (2006) Control of enterotoxin gene expression in Bacillus cereus F4430/73 involves the redox-sensitive ResDE signal transduction system. J Bacteriol 188 : 6640 6651.
17. Durbin, R., Eddy, S., Krogh, A. Mitchison, G. (1998) Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids. Cambridge, UK : Cambridge University Press.
18. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 : 1792 1797.
19. Fagerlund, A., Brillard, J., Fürst, R., Guinebretière, M.H. Granum, P.E. (2007) Toxin production in a rare and genetically remote cluster of strains of the Bacillus cereus group. BMC Microbiol 7 : 43.
20. Francke, C., Kerkhoven, R., Wels, M. Siezen, R.J. (2008) A generic approach to identify Transcription Factor-specific operator motifs; inferences for LacI-family mediated regulation in Lactobacillus plantarum WCFS1. BMC Genomics 9 : 145.
21. Galperin, M.Y. (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188 : 4169 4182.
22. Geng, H., Zhu, Y., Mullen, K., Zuber, C.S. Nakano, M.M. (2007) Characterization of ResDE-dependent fnr transcription in Bacillus subtilis. J Bacteriol 189 : 1745 1755.
23. Grebe, T.W. Stock, J.B. (1999) The histidine protein kinase superfamily. Adv Microb Physiol 41 : 139 227.
24. van der Heijden, R.T., Snel, B., van Noort, V. Huynen, M.A. (2007) Orthology prediction at scalable resolution by phylogenetic tree analysis. BMC Bioinformatics 8 : 83.
25. Herbert, S., Bera, A., Nerz, C., Kraus, D., Peschel, A., Goerke, C., et al. (2007) Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog 3 : e102.
26. Howell, A., Dubrac, S., Andersen, K.K., Noone, D., Fert, J., Msadek, T. Devine, K. (2003) Genes controlled by the essential YycG/YycF two-component system of Bacillus subtilis revealed through a novel hybrid regulator approach. Mol Microbiol 49 : 1639 1655.
27. Jensen, G.B., Hansen, B.M., Eilenberg, J. Mahillon, J. (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5 : 631 640.
28. Jiang, M., Shao, W., Perego, M. Hoch, J.A. (2000) Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol 38 : 535 542.
29. Jordan, S., Junker, A., Helmann, J.D. Mascher, T. (2006) Regulation of LiaRS-dependent gene expression in Bacillus subtilis: identification of inhibitor proteins, regulator binding sites, and target genes of a conserved cell envelope stress-sensing two-component system. J Bacteriol 188 : 5153 5166.
30. Joseph, P., Fichant, G., Quentin, Y. Denizot, F. (2002) Regulatory relationship of two-component and ABC transport systems and clustering of their genes in the Bacillus/Clostridium group, suggest a functional link between them. J Mol Microbiol Biotechnol 4 : 503 513.
31. Joseph, P., Guiseppi, A., Sorokin, A. Denizot, F. (2004) Characterization of the Bacillus subtilis YxdJ response regulator as the inducer of expression for the cognate ABC transporter YxdLM. Microbiology 150 : 2609 2617.
32. Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y. Hattori, M. (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32 : D277 D280.
33. Kerkhoven, R., van Enckevort, F.H., Boekhorst, J., Molenaar, D. Siezen, R.J. (2004) Visualization for genomics: the Microbial Genome Viewer. Bioinformatics 20 : 1812 1814.
34. Kern, D., Volkman, B.F., Luginbühl, P., Nohaile, M.J., Kustu, S. Wemmer, D.E. (1999) Structure of a transiently phosphorylated switch in bacterial signal transduction. Nature 402 : 894 898.
35. Koenig, R.L., Ray, J.L., Maleki, S.J., Smeltzer, M.S. Hurlburt, B.K. (2004) Staphylococcus aureus AgrA binding to the RNAIII-agr regulatory region. J Bacteriol 186 : 7549 7555.
36. Körner, H., Sofia, H.J. Zumft, W.G. (2003) Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 27 : 559 592.
37. Lewis, R.J., Krzywda, S., Brannigan, J.A., Turkenburg, J.P., Muchová, K., Dodson, E.J., et al. (2000) The trans-activation domain of the sporulation response regulator Spo0A revealed by X-ray crystallography. Mol Microbiol 38 : 198 212.
38. Li, M., Lai, Y., Villaruz, A.E., Cha, D.J., Sturdevant, D.E. Otto, M. (2007) Gram-positive three-component antimicrobial peptide-sensing system. Proc Natl Acad Sci USA 104 : 9469 9474.
39. Liu, J., Tan, K. Stormo, G.D. (2003) Computational identification of the Spo0A-phosphate regulon that is essential for the cellular differentiation and development in Gram-positive spore-forming bacteria. Nucleic Acids Res 31 : 6891 6903.
40. Liu, W., Qi, Y. Hulett, F.M. (1998) Sites internal to the coding regions of phoA and pstS bind PhoP and are required for full promoter activity. Mol Microbiol 28 : 119 130.
41. Lyon, G.J. Novick, R.P. (2004) Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25 : 1389 1403.
42. Makita, Y., Nakao, M., Ogasawara, N. Nakai, K. (2004) DBTBS: database of transcriptional regulation in Bacillus subtilis and its contribution to comparative genomics. Nucleic Acids Res 32 : D75 D77.
43. Malvar, T., Gawron-Burke, C. Baum, J.A. (1994) Overexpression of Bacillus thuringiensis HknA, a histidine protein kinase homology, bypasses early Spo mutations that result in CryIIIA overproduction. J Bacteriol 176 : 4742 4749.
44. Mandin, P., Fsihi, H., Dussurget, O., Vergassola, M., Milohanic, E., Toledo-Arana, A., et al. (2005) VirR, a response regulator critical for Listeria monocytogenes virulence. Mol Microbiol 57 : 1367 1380.
45. 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.
46. Martínez-Hackert, E. Stock, A.M. (1997) Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269 : 301 312.
47. Mascher, T., Margulis, N.G., Wang, T., Ye, R.W. Helmann, J.D. (2003) Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol Microbiol 50 : 1591 1604.
48. Mascher, T., Zimmer, S.L., Smith, T.A. Helmann, J.D. (2004) Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob Agents Chemother 48 : 2888 2896.
49. Meehl, M., Herbert, S., Götz, F. Cheung, A. (2007) Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus. Antimicrob Agents Chemother 51 : 2679 2689.
50. Molle, V., Fujita, M., Jensen, S.T., Eichenberger, P., González-Pastor, J.E., Liu, J.S. Losick, R. (2003) The Spo0A regulon of Bacillus subtilis. Mol Microbiol 50 : 1683 1701.
51. Mwangi, M.M. Siggia, E.D. (2003) Genome wide identification of regulatory motifs in Bacillus subtilis. BMC Bioinformatics 4 : 18.
52. Neumüller, A.M., Konz, D. Marahiel, M.A. (2001) The two-component regulatory system BacRS is associated with bacitracin 'self-resistance' of Bacillus licheniformis ATCC 10716. Eur J Biochem 268 : 3180 3189.
53. Ohki, R., Giyanto, Tateno, K., Masuyama, W., Moriya, S., Kobayashi, K. Ogasawara, N. (2003) The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Mol Microbiol 49 : 1135 1144.
54. Overbeek, R., Fonstein, M., D'Souza, M., Pusch, G.D. Maltsev, N. (1999) The use of gene clusters to infer functional coupling. Proc Natl Acad Sci USA 96 : 2896 2901.
55. Pelton, J.G., Kustu, S. Wemmer, D.E. (1999) Solution structure of the DNA-binding domain of NtrC with three alanine substitutions. J Mol Biol 292 : 1095 1110.
56. Pietiäinen, M., Gardemeister, M., Mecklin, M., Leskelä, S., Sarvas, M. Kontinen, V.P. (2005) Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems. Microbiology 151 : 1577 1592.
57. Podlesek, Z., Comino, A., Herzog-Velikonja, B., Zgur-Bertok, D., Komel, R. Grabnar, M. (1995) Bacillus licheniformis bacitracin-resistance ABC transporter: relationship to mammalian multidrug resistance. Mol Microbiol 16 : 969 976.
58. Rasko, D.A., Altherr, M.R., Han, C.S. Ravel, J. (2005) Genomics of the Bacillus cereus group of organisms. FEMS Microbiol Rev 29 : 303 329.
59. Rhee, S., Martin, R.G., Rosner, J.L. Davies, D.R. (1998) A novel DNA-binding motif in MarA: the first structure for an AraC family transcriptional activator. Proc Natl Acad Sci USA 95 : 10413 10418.
60. Satomura, T., Shimura, D., Asai, K., Sadaie, Y., Hirooka, K. Fujita, Y. (2005) Enhancement of glutamine utilization in Bacillus subtilis through the GlnK-GlnL two-component regulatory system. J Bacteriol 187 : 4813 4821.
61. B activity in Bacillus cereus. J Bacteriol 187 : 5846 5851.
62. Schultz, J., Milpetz, F., Bork, P. Ponting, C.P. (1998) smart, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95 : 5857 5864.
63. Serizawa, M. Sekiguchi, J. (2005) The Bacillus subtilis YdfHI two-component system regulates the transcription of ydfJ, a member of the RND superfamily. Microbiology 151 : 1769 1778.
64. Shultzaberger, R.K., Chen, Z., Lewis, K.A. Schneider, T.D. (2007) Anatomy of Escherichia coli sigma70 promoters. Nucleic Acids Res 35 : 771 788.
65. Stauff, D.L., Torres, V.J. Skaar, E.P. (2007) Signaling and DNA-binding activities of the Staphylococcus aureus HssR-HssS two-component system required for heme sensing. J Biol Chem 282 : 26111 26121.
66. Stein, T., Heinzmann, S., Kiesau, P., Himmel, B. Entian, K.D. (2003) The spa-box for transcriptional activation of subtilin biosynthesis and immunity in Bacillus subtilis. Mol Microbiol 47 : 1627 1636.
67. Stock, A.M., Robinson, V.L. Goudreau, P.N. (2000) Two-component signal transduction. Annu Rev Biochem 69 : 183 215.
68. Strauch, M.A., Trach, K.A., Day, J. Hoch, J.A. (1992) Spo0A activates and represses its own synthesis by binding at its dual promoters. Biochimie 74 : 619 626.
69. Sun, G., Birkey, S.M. Hulett, F.M. (1996) Three two-component signal-transduction systems interact for Pho regulation in Bacillus subtilis. Mol Microbiol 19 : 941 948.
70. Szurmant, H. Ordal, G.W. (2004) Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68 : 301 319.
71. Tanaka, K., Kobayashi, K. Ogasawara, N. (2003) The Bacillus subtilis YufLM two-component system regulates the expression of the malate transporters MaeN (YufR) and YflS, and is essential for utilization of malate in minimal medium. Microbiology 149 : 2317 2329.
72. Tatusov, R.L., Natale, D.A., Garkavtsev, I.V., Tatusova, T.A., Shankavaram, U.T., Rao, B.S., et al. (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29 : 22 28.
73. Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 : 4673 4680.
74. Vetter, S.M. Schlievert, P.M. (2007) The two-component system Bacillus respiratory response A and B (BrrA-BrrB) is a virulence factor regulator in Bacillus anthracis. Biochemistry 46 : 7343 7352.
75. Wels, M., Francke, C., Kerkhoven, R., Kleerebezem, M. Siezen, R.J. (2006) Predicting cis-acting elements of Lactobacillus plantarum by comparative genomics with different taxonomic subgroups. Nucleic Acids Res 34 : 1947 1958.
76. Yamamoto, H., Murata, M. Sekiguchi, J. (2000) The CitST two-component system regulates the expression of the Mg-citrate transporter in Bacillus subtilis. Mol Microbiol 37 : 898 912.
77. Yeats, C., Rawlings, N.D. Bateman, A. (2004) The PepSY domain: a regulator of peptidase activity in the microbial environment? Trends Biochem Sci 29 : 169 172.
78. Zigha, A., Rosenfeld, E., Schmitt, P. Duport, C. (2007) The redox regulator Fnr is required for fermentative growth and enterotoxin synthesis in Bacillus cereus F4430/73. J Bacteriol 189 : 2813 2824.