A pivotal role for the response regulator DegU in controlling multicellular behaviour

References

1. Albano M., Smits W. K., Ho L. T., Kraigher B., Mandic-Mulec I., Kuipers O. P., Dubnau D. 2005; The Rok protein of Bacillus subtilis represses genes for cell surface and extracellular functions. J Bacteriol 187:2010–2019
   [Google Scholar]
2. Amati G., Bisicchia P., Galizzi A. 2004; DegU-P represses expression of the motility fla-che operon in Bacillus subtilis . J Bacteriol 186:6003–6014
   [Google Scholar]
3. Branda S. S., Gonzalez-Pastor J. E., Ben-Yehuda S., Losick R., Kolter R. 2001a; Fruiting body formation by Bacillus subtilis . Proc Natl Acad Sci U S A 98:11621–11626
   [Google Scholar]
4. Branda S. S., Chu F., Kearns D. B., Losick R., Kolter R. 2006; A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229–1238
   [Google Scholar]
5. Britton R. A., Eichenberger P., Gonzalez-Pastor J. E., Fawcett P., Monson R., Losick R., Grossman A. D. 2002; Genome-wide analysis of the stationary-phase sigma factor (Sigma-H) regulon of Bacillus subtilis . J Bacteriol 184:4881–4890
   [Google Scholar]
6. Chai Y., Chu F., Kolter R., Losick R. 2008; Bistability and biofilm formation in Bacillus subtilis . Mol Microbiol 67:254–263
   [Google Scholar]
7. Claessen D., de Jong W., Dijkhuizen L., Wosten H. A. 2006; Regulation of Streptomyces development: reach for the sky!. Trends Microbiol 14:313–319
   [Google Scholar]
8. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M. 1995; Microbial biofilms. Annu Rev Microbiol 49:711–745
   [Google Scholar]
9. Dahl M. K., Msadek T., Kunst F., Rapoport G. 1992; The phosphorylation state of the DegU response regulator acts as a molecular switch allowing either degradative enzyme synthesis or expression of genetic competence in Bacillus subtilis . J Biol Chem 267:14509–14514
   [Google Scholar]
10. Dervyn E., Noirot-Gros M. F., Mervelet P., McGovern S., Ehrlich S. D., Polard P., Noirot P. 2004; The bacterial condensin/cohesin-like protein complex acts in DNA repair and regulation of gene expression. Mol Microbiol 51:1629–1640
    [Google Scholar]
11. Dubnau D., Hahn J., Roggiani M., Piazza F., Weinrauch Y. 1994; Two-component regulators and genetic competence in Bacillus subtilis . Res Microbiol 145:403–411
    [Google Scholar]
12. Earl A. M., Losick R., Kolter R. 2007; Bacillus subtilis genome diversity. J Bacteriol 189:1163–1170
    [Google Scholar]
13. Earl A. M., Losick R., Kolter R. 2008; Ecology and genomics of Bacillus subtilis . Trends Microbiol 16:269–275
    [Google Scholar]
14. Fujita M., Gonzalez-Pastor J. E., Losick R. 2005; High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis . J Bacteriol 187:1357–1368
    [Google Scholar]
15. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P. other authors 2001; Comparative genomics of Listeria species. Science 294:849–852
    [Google Scholar]
16. Gueriri I., Bay S., Dubrac S., Cyncynatus C., Msadek T. 2008a; 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
    [Google Scholar]
17. Gueriri I., Cyncynatus C., Dubrac S., Arana A. T., Dussurget O., Msadek T. 2008b; The DegU orphan response regulator of Listeria monocytogenes autorepresses its own synthesis and is required for bacterial motility, virulence and biofilm formation. Microbiology 154:2251–2264
    [Google Scholar]
18. Hamoen L. W., Van Werkhoven A. F., Venema G., Dubnau D. 2000; The pleiotropic response regulator DegU functions as a priming protein in competence development in Bacillus subtilis . Proc Natl Acad Sci U S A 97:9246–9251
    [Google Scholar]
19. Hamoen L. W., Venema G., Kuipers O. P. 2003; Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology 149:9–17
    [Google Scholar]
20. Hamon M. A., Lazazzera B. A. 2001; The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis . Mol Microbiol 42:1199–1209
    [Google Scholar]
21. Kaplan H. B. 2003; Multicellular development and gliding motility in Myxococcus xanthus . Curr Opin Microbiol 6:572–577
    [Google Scholar]
22. Kearns D. B., Losick R. 2003; Swarming motility in undomesticated Bacillus subtilis . Mol Microbiol 49:581–590
    [Google Scholar]
23. Kearns D. B., Losick R. 2005; Cell population heterogeneity during growth of Bacillus subtilis . Genes Dev 19:3083–3094
    [Google Scholar]
24. Kearns D. B., Chu F., Rudner R., Losick R. 2004; Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility. Mol Microbiol 52:357–369
    [Google Scholar]
25. Klein A. H., Shulla A., Reimann S. A., Keating D. H., Wolfe A. J. 2007; The intracellular concentration of acetyl phosphate in Escherichia coli is sufficient for direct phosphorylation of two-component response regulators. J Bacteriol 189:5574–5581
    [Google Scholar]
26. Knudsen G. M., Olsen J. E., Dons L. 2004; Characterization of DegU, a response regulator in Listeria monocytogenes, involved in regulation of motility and contributes to virulence. FEMS Microbiol Lett 240:171–179
    [Google Scholar]
27. Kobayashi K. 2007; Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis . Mol Microbiol 66:395–409
    [Google Scholar]
28. Kobayashi K. 2008; SlrR/SlrA control the initiation of biofilm formation in Bacillus subtilis . Mol Microbiol 69:1399–1410
    [Google Scholar]
29. Kunst F., Msadek T., Bignon J., Rapoport G. 1994; The DegS/DegU and ComP/ComA two-component systems are part of a network controlling degradative enzyme synthesis and competence in Bacillus subtilis . Res Microbiol 145:393–402
    [Google Scholar]
30. Laub M. T., Goulian M. 2007; Specificity in two-component signal transduction pathways. Annu Rev Genet 41:121–145
    [Google Scholar]
31. Lazazzera B. A., Palmer T., Quisel J. D., Grossman A. D. 1999; Cell density control of gene expression and development in Bacillus subtilis . In Cell–Cell Signaling in Bacteria pp 27–46 Edited by Dunny G. M., Winas S. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
32. Lemon K. P., Higgins D. E., Kolter R. 2007; Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189:4418–4424
    [Google Scholar]
33. Losick R., Desplan C. 2008; Stochasticity and cell fate. Science 320:65–68
    [Google Scholar]
34. Macek B., Mijakovic I., Olsen J. V., Gnad F., Kumar C., Jensen P. R., Mann M. 2007; The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis . Mol Cell Proteomics 6:697–707
    [Google Scholar]
35. Mader U., Antelmann H., Buder T., Dahl M. K., Hecker M., Homuth G. 2002; Bacillus subtilis functional genomics: genome-wide analysis of the DegS–DegU regulon by transcriptomics and proteomics. Mol Genet Genomics 268:455–467
    [Google Scholar]
36. Mascher T., Helmann J. D., Unden G. 2006; Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70:910–938
    [Google Scholar]
37. Mauder N., Williams T., Fritsch F., Kuhn M., Beier D. 2008; Response regulator DegU of Listeria monocytogenes controls temperature-responsive flagellar gene expression in its unphosphorylated state. J Bacteriol 190:4777–4781
    [Google Scholar]
38. Morikawa M., Kagihiro S., Haruki M., Takano K., Branda S., Kolter R., Kanaya S. 2006; Biofilm formation by a Bacillus subtilis strain that produces γ-polyglutamate. Microbiology 152:2801–2807
    [Google Scholar]
39. 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
    [Google Scholar]
40. Msadek T., Kunst F., Klier A., Rapoport G. 1991; DegS–DegU and ComP–ComA modulator–effector pairs control expression of the Bacillus subtilis pleiotropic regulatory gene degQ . J Bacteriol 173:2366–2377
    [Google Scholar]
41. Ogura M., Tanaka T. 1996; Bacillus subtilis DegU acts as a positive regulator for comK expression. FEBS Lett 397:173–176
    [Google Scholar]
42. Ogura M., Yamaguchi H., Yoshida K., Fujita Y., Tanaka T. 2001; DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B. subtilis two-component regulatory systems. Nucleic Acids Res 29:3804–3813
    [Google Scholar]
43. Ogura M., Shimane K., Asai K., Ogasawara N., Tanaka T. 2003; Binding of response regulator DegU to the aprE promoter is inhibited by RapG, which is counteracted by extracellular PhrG in Bacillus subtilis . Mol Microbiol 49:1685–1697
    [Google Scholar]
44. Piggot P. J., Hilbert D. W. 2004; Sporulation of Bacillus subtilis . Curr Opin Microbiol 7:579–586
    [Google Scholar]
45. Shapiro J. A. 1998; Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104
    [Google Scholar]
46. Shen A., Higgins D. E. 2006; The MogR transcriptional repressor regulates nonhierarchal expression of flagellar motility genes and virulence in Listeria monocytogenes . PLoS Pathog 2:e30
    [Google Scholar]
47. Shen A., Kamp H. D., Grundling A., Higgins D. E. 2006; A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev 20:3283–3295
    [Google Scholar]
48. Smits W. K., Hoa T. T., Hamoen L. W., Kuipers O. P., Dubnau D. 2007; Antirepression as a second mechanism of transcriptional activation by a minor groove binding protein. Mol Microbiol 64:368–381
    [Google Scholar]
49. Spizizen J. 1958; Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci U S A 44:1072–1078
    [Google Scholar]
50. Srivatsan A., Han Y., Peng J., Tehranchi A. K., Gibbs R., Wang J. D., Chen R. 2008; High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet 4:e1000139
    [Google Scholar]
51. Stanley N. R., Lazazzera B. A. 2005; Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly- γ-dl-glutamic acid production and biofilm formation. Mol Microbiol 57:1143–1158
    [Google Scholar]
52. Tanaka T., Kawata M., Mukai K. 1991; Altered phosphorylation of Bacillus subtilis DegU caused by single amino acid changes in DegS. J Bacteriol 173:5507–5515
    [Google Scholar]
53. Tsukahara K., Ogura M. 2008; Promoter selectivity of the Bacillus subtilis response regulator DegU, a positive regulator of the fla/che operon and sacB . BMC Microbiol 8:8
    [Google Scholar]
54. Veening J. W., Smits W. K., Hamoen L. W., Jongbloed J. D., Kuipers O. P. 2004; Visualization of differential gene expression by improved cyan fluorescent protein and yellow fluorescent protein production in Bacillus subtilis . Appl Environ Microbiol 70:6809–6815
    [Google Scholar]
55. Veening J. W., Hamoen L. W., Kuipers O. P. 2005; Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis . Mol Microbiol 56:1481–1494
    [Google Scholar]
56. Veening J. W., Igoshin O. A., Eijlander R. T., Nijland R., Hamoen L. W., Kuipers O. P. 2008a; Transient heterogeneity in extracellular protease production by Bacillus subtilis . Mol Syst Biol 4:184
    [Google Scholar]
57. Veening J. W., Smits W. K., Kuipers O. P. 2008b; Bistability, epigenetics, and bet-hedging in Bacteria. Annu Rev Microbiol 62:193–210
    [Google Scholar]
58. Verhamme D. T., Kiley T. B., Stanley-Wall N. R. 2007; DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis . Mol Microbiol 65:554–568
    [Google Scholar]
59. Verhamme D. T., Murray E. J., Stanley-Wall N. R. 2008; DegU and Spo0A jointly control transcription of two loci required for complex colony development by Bacillus subtilis . J BacteriolOct 31: [Epub ahead of print]
    [Google Scholar]
60. Vlamakis H., Aguilar C., Losick R., Kolter R. 2008; Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev 22:945–953
    [Google Scholar]
61. Williams T., Bauer S., Beier D., Kuhn M. 2005a; Construction and characterization of Listeria monocytogenes mutants with in-frame deletions in the response regulator genes identified in the genome sequence. Infect Immun 73:3152–3159
    [Google Scholar]
62. Williams T., Joseph B., Beier D., Goebel W., Kuhn M. 2005b; Response regulator DegU of Listeria monocytogenes regulates the expression of flagella-specific genes. FEMS Microbiol Lett 252:287–298
    [Google Scholar]
63. Wolfe A. J. 2005; The acetate switch. Microbiol Mol Biol Rev 69:12–50
    [Google Scholar]
64. Wolfe A. J., Chang D. E., Walker J. D., Seitz-Partridge J. E., Vidaurri M. D., Lange C. F., Prüss B. M., Henk M. C., Larkin J. C., Conway T. (2003; Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol 48:977–988
    [Google Scholar]
65. Wolfe A. J., Parikh N., Lima B. P., Zemaitaitis B. 2008; Signal integration by the two-component signal transduction response regulator CpxR. J Bacteriol 190:2314–2322
    [Google Scholar]
66. Yasumura A., Abe S., Tanaka T. 2008; Involvement of nitrogen regulation in Bacillus subtilis degU expression. J Bacteriol 190:5162–5171
    [Google Scholar]
67. Zeigler D. R., Pragai Z., Rodriguez S., Chevreux B., Muffler A., Albert T., Bai R., Wyss M., Perkins J. B. 2008; The origins of 168, W23, and other Bacillus subtilis legacy strains. J Bacteriol 190:6983–6995
    [Google Scholar]