1887

Abstract

Bacteria control multicellular behavioural responses, including biofilm formation and swarming motility, by integrating environmental cues through a complex regulatory network. Heterogeneous gene expression within an otherwise isogenic cell population that allows for differentiation of cell fate is an intriguing phenomenon that adds to the complexity of multicellular behaviour. This review focuses on recent data about how DegU, a pleiotropic response regulator, co-ordinates multicellular behaviour in . We review studies that challenge the conventional understanding of the molecular mechanisms underpinning the DegU regulatory system and others that describe novel targets of DegU during activation of biofilm formation by . We also discuss a novel role for DegU in regulating multicellular processes in the food-borne pathogen .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.023903-0
2009-01-01
2020-06-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/1/1.html?itemId=/content/journal/micro/10.1099/mic.0.023903-0&mimeType=html&fmt=ahah

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 Bacteriol187:2010–2019
    [Google Scholar]
  2. Amati G., Bisicchia P., Galizzi A.. 2004; DegU-P represses expression of the motility fla-che operon in Bacillus subtilis. J Bacteriol186:6003–6014
    [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 A98:11621–11626
    [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 Microbiol59:1229–1238
    [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 Bacteriol184:4881–4890
    [Google Scholar]
  6. Chai Y., Chu F., Kolter R., Losick R.. 2008; Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol67:254–263
    [Google Scholar]
  7. Claessen D., de Jong W., Dijkhuizen L., Wosten H. A.. 2006; Regulation of Streptomyces development: reach for the sky!. Trends Microbiol14:313–319
    [Google Scholar]
  8. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M.. 1995; Microbial biofilms. Annu Rev Microbiol49:711–745
    [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 Chem267:14509–14514
    [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 Microbiol51:1629–1640
    [Google Scholar]
  11. Dubnau D., Hahn J., Roggiani M., Piazza F., Weinrauch Y.. 1994; Two-component regulators and genetic competence in Bacillus subtilis. Res Microbiol145:403–411
    [Google Scholar]
  12. Earl A. M., Losick R., Kolter R.. 2007; Bacillus subtilis genome diversity. J Bacteriol189:1163–1170
    [Google Scholar]
  13. Earl A. M., Losick R., Kolter R.. 2008; Ecology and genomics of Bacillus subtilis. Trends Microbiol16:269–275
    [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 Bacteriol187:1357–1368
    [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. Science294:849–852
    [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. Microbiology154:2251–2264
    [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 A97:9246–9251
    [Google Scholar]
  19. Hamoen L. W., Venema G., Kuipers O. P.. 2003; Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology149:9–17
    [Google Scholar]
  20. Hamon M. A., Lazazzera B. A.. 2001; The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol42:1199–1209
    [Google Scholar]
  21. Kaplan H. B.. 2003; Multicellular development and gliding motility in Myxococcus xanthus. Curr Opin Microbiol6:572–577
    [Google Scholar]
  22. Kearns D. B., Losick R.. 2003; Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol49:581–590
    [Google Scholar]
  23. Kearns D. B., Losick R.. 2005; Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev19:3083–3094
    [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 Microbiol52:357–369
    [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 Bacteriol189:5574–5581
    [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 Lett240:171–179
    [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 Microbiol66:395–409
    [Google Scholar]
  28. Kobayashi K.. 2008; SlrR/SlrA control the initiation of biofilm formation in Bacillus subtilis. Mol Microbiol69:1399–1410
    [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 Microbiol145:393–402
    [Google Scholar]
  30. Laub M. T., Goulian M.. 2007; Specificity in two-component signal transduction pathways. Annu Rev Genet41:121–145
    [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 pp27–46 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 Bacteriol189:4418–4424
    [Google Scholar]
  33. Losick R., Desplan C.. 2008; Stochasticity and cell fate. Science320:65–68
    [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 Proteomics6:697–707
    [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 Genomics268:455–467
    [Google Scholar]
  36. Mascher T., Helmann J. D., Unden G.. 2006; Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev70:910–938
    [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 Bacteriol190:4777–4781
    [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. Microbiology152:2801–2807
    [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 Bacteriol172:824–834
    [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 Bacteriol173:2366–2377
    [Google Scholar]
  41. Ogura M., Tanaka T.. 1996; Bacillus subtilis DegU acts as a positive regulator for comK expression. FEBS Lett397:173–176
    [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 Res29:3804–3813
    [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 Microbiol49:1685–1697
    [Google Scholar]
  44. Piggot P. J., Hilbert D. W.. 2004; Sporulation of Bacillus subtilis. Curr Opin Microbiol7:579–586
    [Google Scholar]
  45. Shapiro J. A.. 1998; Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol52:81–104
    [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 Pathog2: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 Dev20:3283–3295
    [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 Microbiol64:368–381
    [Google Scholar]
  49. Spizizen J.. 1958; Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci U S A44:1072–1078
    [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 Genet4: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 Microbiol57:1143–1158
    [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 Bacteriol173:5507–5515
    [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 Microbiol8:8
    [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 Microbiol70:6809–6815
    [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 Microbiol56:1481–1494
    [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 Biol4:184
    [Google Scholar]
  57. Veening J. W., Smits W. K., Kuipers O. P.. 2008b; Bistability, epigenetics, and bet-hedging in Bacteria. Annu Rev Microbiol62:193–210
    [Google Scholar]
  58. Verhamme D. T., Kiley T. B., Stanley-Wall N. R.. 2007; DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol Microbiol65:554–568
    [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 BacteriolOct31: [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 Dev22:945–953
    [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 Immun73:3152–3159
    [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 Lett252:287–298
    [Google Scholar]
  63. Wolfe A. J.. 2005; The acetate switch. Microbiol Mol Biol Rev69:12–50
    [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 Microbiol48:977–988
    [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 Bacteriol190:2314–2322
    [Google Scholar]
  66. Yasumura A., Abe S., Tanaka T.. 2008; Involvement of nitrogen regulation in Bacillus subtilis degU expression. J Bacteriol190:5162–5171
    [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 Bacteriol190:6983–6995
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.023903-0
Loading
/content/journal/micro/10.1099/mic.0.023903-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error