1887

Abstract

The soil bacterium frequently encounters a reduction in temperature in its natural habitats. Here, a combined transcriptomic and proteomic approach has been used to analyse the adaptational responses of to low temperature. Propagation of in minimal medium at 15 °C triggered the induction of 279 genes and the repression of 301 genes in comparison to cells grown at 37 °C. The analysis thus revealed profound adjustments in the overall gene expression profile in chill-adapted cells. Important transcriptional changes in low-temperature-grown cells comprise the induction of the SigB-controlled general stress regulon, the induction of parts of the early sporulation regulons (SigF, SigE and SigG) and the induction of a regulatory circuit (RapA/PhrA and Opp) that is involved in the fine-tuning of the phosphorylation status of the Spo0A response regulator. The analysis of chill-stress-repressed genes revealed reductions in major catabolic (glycolysis, oxidative phosphorylation, ATP synthesis) and anabolic routes (biosynthesis of purines, pyrimidines, haem and fatty acids) that likely reflect the slower growth rates at low temperature. Low-temperature repression of part of the SigW regulon and of many genes with predicted functions in chemotaxis and motility was also noted. The proteome analysis of chill-adapted cells indicates a major contribution of post-transcriptional regulation phenomena in adaptation to low temperature. Comparative analysis of the previously reported transcriptional responses of cold-shocked cells with this data revealed that cold shock and growth in the cold constitute physiologically distinct phases of the adaptation of to low temperature.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28530-0
2006-03-01
2020-07-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/3/831.html?itemId=/content/journal/micro/10.1099/mic.0.28530-0&mimeType=html&fmt=ahah

References

  1. Aguilar P. S, Cronan J. E, de Mendoza D Jr. 1998; A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. J Bacteriol180:2194–2200
    [Google Scholar]
  2. Aguilar P. S, Lopez P, De Mendoza D. 1999; Transcriptional control of the low-temperature-inducible des gene, encoding the Δ5 desaturase of Bacillus subtilis . J Bacteriol181:7028–7033
    [Google Scholar]
  3. 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 J20:1681–1691[CrossRef]
    [Google Scholar]
  4. Aizawa S. I, Zhulin I. B, Marquez-Magana L. M, Ordal G. W. 2002; Chemotaxis and motility. In Bacillus subtilis and its Closest Relatives: from Genes to Cells pp 437–452 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  5. Amati G, Bisicchia P, Galizzi A. 2004; DegU-P represses expression of the motility fla - che operon in Bacillus subtilis . J Bacteriol186:6003–6014[CrossRef]
    [Google Scholar]
  6. Amaya E, Khvorova A, Piggot P. J. 2001; Analysis of promoter recognition in vivo directed by σ [sup]F[/sup] of Bacillus subtilis by using random-sequence oligonucleotides. J Bacteriol183:3623–3630[CrossRef]
    [Google Scholar]
  7. Beckering C. L, Steil L, Weber M. H, Völker U, Marahiel M. A. 2002; Genomewide transcriptional analysis of the cold shock response in Bacillus subtilis . J Bacteriol184:6395–6402[CrossRef]
    [Google Scholar]
  8. Benson A. K, Haldenwang W. G. 1993; The σ [sup]B[/sup] dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock. J Bacteriol175:1929–1935
    [Google Scholar]
  9. Berka R. M, Hahn J, Albano M, Draskovic I, Persuh M, Cui X, Sloma A, Widner W, Dubnau D. 2002; Microarray analysis of the Bacillus subtilis K-state: genome-wide expression changes dependent on ComK. Mol Microbiol43:1331–1345[CrossRef]
    [Google Scholar]
  10. Bongiorni C, Ishikawa S, Stephenson S, Ogasawara N, Perego M. 2005; Synergistic regulation of competence development in Bacillus subtilis by two Rap-Phr systems. J Bacteriol187:4353–4361[CrossRef]
    [Google Scholar]
  11. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72:248–254[CrossRef]
    [Google Scholar]
  12. Bremer E. 2002; Adaptation to changing osmolarity. In Bacillus subtilis and its Closest Relatives: from Genes to Cells pp 385–391 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  13. Brigulla M, Hoffmann T, Krisp A, Völker A, Bremer E, Völker U. 2003; Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J Bacteriol185:4305–4314[CrossRef]
    [Google Scholar]
  14. Cao M, Kobel P. A, Morshedi M. M, Wu M. F, Paddon C, Helmann J. D. 2002; Defining the Bacillus subtilis σ [sup]W[/sup] regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J Mol Biol316:443–457[CrossRef]
    [Google Scholar]
  15. Core L, Perego M. 2003; TPR-mediated interaction of RapC with ComA inhibits response regulator-DNA binding for competence development in Bacillus subtilis . Mol Microbiol49:1509–1522[CrossRef]
    [Google Scholar]
  16. Dammel C. S, Noller H. F. 1995; Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes Dev9:626–637[CrossRef]
    [Google Scholar]
  17. Eichenberger P, Jensen S. T, Conlon E. M.8 other authors 2003; The σ [sup]E[/sup] regulon and the identification of additional sporulation genes in Bacillus subtilis . J Mol Biol327:945–972[CrossRef]
    [Google Scholar]
  18. Eichenberger P, Fujita M, Jensen S. T.8 other authors 2004; The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis . PLoS Biol2:E328[CrossRef]
    [Google Scholar]
  19. Eymann C, Dreisbach A, Albrecht D.10 other authors 2004; A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics4:2849–2876[CrossRef]
    [Google Scholar]
  20. Fabret C, Feher V. A, Hoch J. A. 1999; Two-component signal transduction in Bacillus subtilis : how one organism sees its world. J Bacteriol181:1975–1983
    [Google Scholar]
  21. Fawcett P, Eichenberger P, Losick R, Youngman P. 2000; The transcriptional profile of early to middle sporulation in Bacillus subtilis . Proc Natl Acad Sci U S A97:8063–8068[CrossRef]
    [Google Scholar]
  22. Feucht A, Evans L, Errington J. 2003; Identification of sporulation genes by genome-wide analysis of the σ [sup]E[/sup] regulon of Bacillus subtilis . Microbiology149:3023–3034[CrossRef]
    [Google Scholar]
  23. Graumann P, Marahiel M. A. 1996; Some like it cold: response of microorganisms to cold shock. Arch Microbiol166:293–300[CrossRef]
    [Google Scholar]
  24. Graumann P, Schröder K, Schmid R, Marahiel M. A. 1996; Cold shock stress-induced proteins in Bacillus subtilis . J Bacteriol178:4611–4619
    [Google Scholar]
  25. Graumann P, Wendrich T. M, Weber M. H. W, Schröder K, Marahiel A. 1997; A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol Microbiol25:741–756[CrossRef]
    [Google Scholar]
  26. Harwood C. R, Archibald A. R. 1990; Growth, maintenance and general techniques. In Molecular Biological Methods for Bacillus pp 1–26 Edited by Harwood C. R., Cutting S. M.. Chichester: Wiley;
    [Google Scholar]
  27. Harwood C. R, Cutting S. M. 1990; Molecular Biological Methods for Bacillus Chichester: Wiley;
    [Google Scholar]
  28. Hauser N. C, Vingron M, Scheideler M, Krems B, Hellmuth K, Entian K. D, Hoheisel J. D. 1998; Transcriptional profiling on all open reading frames of Saccharomyces cerevisiae . Yeast14:1209–1221[CrossRef]
    [Google Scholar]
  29. Hecker M, Völker U. 2001; General stress response of Bacillus subtilis and other bacteria. Adv Microb Physiol44:35–91
    [Google Scholar]
  30. Hecker M, Schumann W, Völker U. 1996; Heat-shock and general stress response in Bacillus subtilis . Mol Microbiol19:417–428[CrossRef]
    [Google Scholar]
  31. Helmann J. D, Moran C. P. 2002; RNA polymerase and sigma factors. In Bacillus subtilis and its Closest Relatives: from Genes to Cells pp 289–312 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  32. Helmann J. D, Wu M. F, Kobel P. A, Gamo F. J, Wilson M, Morshedi M. M, Navre M, Paddon C. 2001; Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol183:7318–7328[CrossRef]
    [Google Scholar]
  33. Hoch J. A. 1995; Control of cellular development in sporulating bacteria by the phosphorelay two-component signal transduction system. In Two-Component Signal Transduction pp 129–144 Edited by Hoch J. A., Silhavy T. J.. Washington DC: American Society for Microbiology;
    [Google Scholar]
  34. Holtmann G, Bremer E. 2004; Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of the Opu transporters. J Bacteriol186:1683–1693[CrossRef]
    [Google Scholar]
  35. Holtmann G, Bakker E. P, Uozumi N, Bremer E. 2003; KtrAB and KtrCD: two K[sup]+[/sup] uptake systems in Bacillus subtilis and their role in the adaptation to hypertonicity. J Bacteriol185:1289–1298[CrossRef]
    [Google Scholar]
  36. Holtmann G, Brigulla M, Steil L, Schütz A, Barnekow K, Völker U, Bremer E. 2004; RsbV-independent induction of the SigB-dependent general stress regulon of Bacillus subtilis during growth at high temperature. J Bacteriol186:6150–6158[CrossRef]
    [Google Scholar]
  37. Honjo M, Nakayama A, Fukazawa K, Kawamura K, Ando K, Hori M, Furutani Y. 1990; A novel Bacillus subtilis gene involved in negative control of sporulation and degradative-enzyme production. J Bacteriol172:1783–1790
    [Google Scholar]
  38. Höper D, Völker U, Hecker M. 2005; Comprehensive characterization of the contribution of individual SigB-dependent general stress genes to stress resistance of Bacillus subtilis . J Bacteriol187:2810–2826[CrossRef]
    [Google Scholar]
  39. Huang X, Fredrick K. L, Helmann J. D. 1998; Promoter recognition by Bacillus subtilis σ [sup]W[/sup]: autoregulation and partial overlap with the σ [sup]X[/sup] regulon. J Bacteriol180:3765–3770
    [Google Scholar]
  40. Igo M, Lampe M, Ray C, Schafer W, Moran C. P, Losick R Jr. 1987; Genetic studies of a secondary RNA polymerase sigma factor in Bacillus subtilis . J Bacteriol169:3464–3469
    [Google Scholar]
  41. Jiang M, Grau R, Perego M. 2000; Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis . J Bacteriol182:303–310[CrossRef]
    [Google Scholar]
  42. Jones P. G, Mitta M, Kim Y, Jiang W. N, Inouye M. 1996; Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli . Proc Natl Acad Sci U S A93:76–80[CrossRef]
    [Google Scholar]
  43. Kaan T, Jürgen B, Schweder T. 1999; Regulation of the expression of the cold shock proteins CspB and CspC in Bacillus subtilis . Mol Gen Genet262:351–354[CrossRef]
    [Google Scholar]
  44. Kaan T, Homuth G, Mäder U, Bandow J, Schweder T. 2002; Genome-wide transcriptional profiling of the Bacillus subtilis cold-shock response. Microbiology148:3441–3455
    [Google Scholar]
  45. Kalman S, Duncan M. L, Thomas S. M, Price C. W. 1990; Similar organization of the sigB and spoIIA operons encoding alternate sigma factors of Bacillus subtilis RNA polymerase. J Bacteriol172:5575–5585
    [Google Scholar]
  46. Kempf B, Bremer E. 1995; OpuA, an osmotically regulated binding protein-dependent transport system for the osmoprotectant glycine betaine in Bacillus subtilis . J Biol Chem270:16701–16713[CrossRef]
    [Google Scholar]
  47. Klein W, Weber M. H. W, Marahiel M. A. 1999; Cold shock response of Bacillus subtilis : isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J Bacteriol181:5341–5349
    [Google Scholar]
  48. Kunst F, Ogasawara N, Moszer I. & 148 other authors. 1997; The complete genome sequence of the Gram-positive bacterium Bacillus subtilis . Nature390:249–256[CrossRef]
    [Google Scholar]
  49. Liu S, Graham J. E, Bigelow L, Morse P. D, Wilkinson B. J 2nd. 2002; Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Appl Environ Microbiol68:1697–1705[CrossRef]
    [Google Scholar]
  50. Mäder 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[CrossRef]
    [Google Scholar]
  51. Mansilla M. C, Cybulski L. E, Albanesi D, de Mendoza D. 2004; Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol186:6681–6688[CrossRef]
    [Google Scholar]
  52. Mendez M. B, Orsaria L. M, Philippe V, Pedrido M. E, Grau R. R. 2004; Novel roles of the master transcription factors Spo0A and σ [sup]B[/sup] for survival and sporulation of Bacillus subtilis at low growth temperature. J Bacteriol186:989–1000[CrossRef]
    [Google Scholar]
  53. Molle V, Fujita M, Jensen S. T, Eichenberger P, Gonzalez-Pastor J. E, Liu J. S, Losick R. 2003a; The Spo0A regulon of Bacillus subtilis . Mol Microbiol50:1683–1701[CrossRef]
    [Google Scholar]
  54. Molle V, Nakaura Y, Shivers R. P, Yamaguchi H, Losick R, Fujita Y, Sonenshein A. L. 2003b; Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol185:1911–1922[CrossRef]
    [Google Scholar]
  55. Moszer I, Jones L. M, Moreira S, Fabry C, Danchin A. 2002; SubtiList: the reference database for the Bacillus subtilis genome. Nucleic Acids Res30:62–65[CrossRef]
    [Google Scholar]
  56. Nichols D. S, Nichols P. D, McMeekin T. A. 1995; Ecology and physiology of psychrophilic bacteria from Antarctic saline lakes and ice-sea. Sci Prog78:311–348
    [Google Scholar]
  57. Nickel M, Homuth G, Bohnisch C, Mader U, Schweder T. 2004; Cold induction of the Bacillus subtilis bkd operon is mediated by increased mRNA stability. Mol Genet Genomics272:98–107
    [Google Scholar]
  58. 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[CrossRef]
    [Google Scholar]
  59. 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[CrossRef]
    [Google Scholar]
  60. Perego M. 1997; A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. Proc Natl Acad Sci U S A94:8612–8617[CrossRef]
    [Google Scholar]
  61. Perego M. 1999; Self-signalling by Phr peptides modulates Bacillus subtilis development. In Cell-Cell Signalling in Bacteria pp 243–258 Edited by Dunny G. M., Winans S. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  62. Perego M, Higgins C. F, Pearce S. R, Gallagher M. P, Hoch J. A. 1991; The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol5:173–185[CrossRef]
    [Google Scholar]
  63. Perego M, Hanstein C, Welsh K. M, Djavakhishvili T, Glaser P, Hoch J. A. 1994; Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis . Cell79:1047–1055[CrossRef]
    [Google Scholar]
  64. Perego M, Glaser P, Hoch J. A. 1996; Aspartyl-phosphate phosphatases deactivate the response regulator components of the sporulation signal transduction system in Bacillus subtilis . Mol Microbiol19:1151–1157[CrossRef]
    [Google Scholar]
  65. Petersohn A, Brigulla M, Haas S, Hoheisel J. D, Völker U, Hecker M. 2001; Global analysis of the general stress response of Bacillus subtilis . J Bacteriol183:5617–5631[CrossRef]
    [Google Scholar]
  66. Price C. W. 2002; General stress response. In Bacillus subtilis and its Closest Relatives: from Genes to Cells pp 369–384 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  67. Price C. W, Fawcett P, Ceremonie H, Su N, Murphy C. K, Youngman P. 2001; Genome-wide analysis of the general stress response in Bacillus subtilis . Mol Microbiol41:757–774
    [Google Scholar]
  68. Schobel S, Zellmeier S, Schumann W, Wiegert T. 2004; The Bacillus subtilis σ [sup]W[/sup] anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol Microbiol52:1091–1105[CrossRef]
    [Google Scholar]
  69. Schumann W, Hecker M, Msadek T. 2002; Regulation and function of heat-inducible genes in Bacillus subtilis. In Bacillus subtilis and its Closest Relatives: from Genes to Cells pp 359–368 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  70. Sonenshein A. L. 2000; Bacterial sporulation: a response to environmental signals. In Bacterial Stress Responses pp 199–215 Edited by Storz G., Hengge-Aronis R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  71. Steil L, Hoffmann T, Budde I, Völker U, Bremer E. 2003; Genome-wide transcriptional profiling analysis of adaptation of Bacillus subtilis to high salinity. J Bacteriol185:6358–6370[CrossRef]
    [Google Scholar]
  72. Steil L, Serrano M, Henriques A. O, Völker U. 2005; Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis . Microbiology151:399–420[CrossRef]
    [Google Scholar]
  73. Stragier P, Losick R. 1996; Molecular genetics of sporulation in Bacillus subtilis . Annu Rev Genet30:297–341[CrossRef]
    [Google Scholar]
  74. Stragier P, Bonamy C, Karmazyn-Campelli C. 1988; Processing of a sporulation sigma factor in Bacillus subtilis : how morphological structure could control gene expression. Cell52:697–704[CrossRef]
    [Google Scholar]
  75. Völker U, Engelmann S, Maul B, Riethdorf S, Völker A, Schmid R, Mach H, Hecker M. 1994; Analysis of the induction of general stress proteins of Bacillus subtilis . Microbiology140:741–752[CrossRef]
    [Google Scholar]
  76. Völker U, Maul B, Hecker M. 1999; Expression of the σ [sup]B[/sup]-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis . J Bacteriol181:3942–3948
    [Google Scholar]
  77. Weber M. H, Marahiel M. A. 2002; Coping with the cold: the cold shock response in the Gram-positive soil bacterium Bacillus subtilis . Philos Trans R Soc Lond Biol Sci357:895–907[CrossRef]
    [Google Scholar]
  78. Weber M. H, Klein W, Müller L, Niess U. M, Marahiel M. A. 2001a; Role of the Bacillus subtilis fatty acid desaturase in membrane adaptation during cold shock. Mol Microbiol39:1321–1329[CrossRef]
    [Google Scholar]
  79. Weber M. H, Volkov A. V, Fricke I, Marahiel M. A, Graumann P. L. 2001b; Localization of cold shock proteins to cytosolic spaces surrounding nucleoids in Bacillus subtilis depends on active transcription. J Bacteriol183:6435–6443[CrossRef]
    [Google Scholar]
  80. Weber M. H, Marahiel M. A. 2003; Bacterial cold shock responses. Sci Prog86:9–75[CrossRef]
    [Google Scholar]
  81. Wiegert T, Homuth G, Versteeg S, Schumann W. 2001; Alkaline shock induces the Bacillus subtilis σ [sup]W[/sup] regulon. Mol Microbiol41:59–71[CrossRef]
    [Google Scholar]
  82. Wipat A, Harwood C. R. 1999; The Bacillus subtilis genome sequence: the molecular blueprint of a soil bacterium. FEMS Microbiol Ecol28:1–9[CrossRef]
    [Google Scholar]
  83. Yoshida K. I, Fujita Y, Ehrlich S. D. 2000; An operon for a putative ATP-binding cassette transport system involved in acetoin utilization of Bacillus subtilis . J Bacteriol182:5454–5461[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28530-0
Loading
/content/journal/micro/10.1099/mic.0.28530-0
Loading

Data & Media loading...

Supplements

MIAME description. [PDF file](41 KB)

PDF

Supplementary Table S2. [PDF file](41 KB)

PDF

Supplementary Table S3. [PDF file](27 KB)

PDF

Supplementary Table S4. [PDF file](25 KB)

PDF

Supplementary Table S5. [PDF file](18 KB)

PDF

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