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PMID: 11717291 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Global transcriptional response of Bacillus subtilis to heat shock.

Journal of bacteriology ·Vol. 183 ·No. 24 ·2001-12-00 ·Pages 7318-28

Helmann JD, Wu MF, Kobel PA, Gamo FJ, Wilson M, Morshedi MM, Navre M, Paddon C

Abstract

In response to heat stress, Bacillus subtilis activates the transcription of well over 100 different genes. Many of these genes are members of a general stress response regulon controlled by the secondary sigma factor, sigma(B), while others are under control of the HrcA or CtsR heat shock regulators. We have used DNA microarrays to monitor the global transcriptional response to heat shock. We find strong induction of known sigma(B)-dependent genes with a characteristic rapid induction followed by a return to near prestimulus levels. The HrcA and CtsR regulons are also induced, but with somewhat slower kinetics. Analysis of DNA sequences proximal to newly identified heat-induced genes leads us to propose ~70 additional members of the sigma(B) regulon. We have also identified numerous heat-induced genes that are not members of known heat shock regulons. Notably, we observe very strong induction of arginine biosynthesis and transport operons. Induction of several genes was confirmed by quantitative reverse transcriptase PCR. In addition, the transcriptional responses measured by microarray hybridization compare favorably with the numerous previous studies of heat shock in this organism. Since many different conditions elicit both specific and general stress responses, knowledge of the heat-induced general stress response reported here will be helpful for interpreting future microarray studies of other stress responses.

MeSH Terms
Arginine/metabolism Bacillus subtilis/genetics Bacterial Proteins/genetics Base Sequence DNA-Binding Proteins Gene Expression Profiling Gene Expression Regulation, Bacterial Genes, Bacterial Heat-Shock Response/genetics Molecular Sequence Data Oligonucleotide Array Sequence Analysis Operon Regulon Repressor Proteins/genetics Sigma Factor/genetics Transcription, Genetic
Chemicals
Bacterial Proteins DNA-Binding Proteins Repressor Proteins SigB protein, Bacteria Sigma Factor Arginine
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Helmann J D
Department of Microbiology, Cornell University, Ithaca, New York 14853-8101, USA. [email protected]
Wu M F
Kobel P A
Gamo F J
Wilson M
Morshedi M M
Navre M
Paddon C
References (66)
66 references, click to expand
  1. ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis.
    Mol Microbiol. 1999 May;32(3):581-93 PMID: 10320580
  2. Global gene expression profiling in Escherichia coli K12. The effects of integration host factor.
    J Biol Chem. 2000 Sep 22;275(38):29672-84 PMID: 10871608
  3. Proteomics, DNA arrays and the analysis of still unknown regulons and unknown proteins of Bacillus subtilis and pathogenic gram-positive bacteria.
    Int J Med Microbiol. 2000 May;290(2):123-34 PMID: 11045917
  4. Four additional genes in the sigB operon of Bacillus subtilis that control activity of the general stress factor sigma B in response to environmental signals.
    J Bacteriol. 1995 Jan;177(1):123-33 PMID: 8002610
  5. Extracting biological information from DNA arrays: an unexpected link between arginine and methionine metabolism in Bacillus subtilis.
    Genome Biol. 2001;2(6):RESEARCH0019 PMID: 11423008
  6. Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media.
    J Bacteriol. 1999 Oct;181(20):6425-40 PMID: 10515934
  7. The act operon controls the level and time of C-signal production for Myxococcus xanthus development.
    Mol Microbiol. 2001 May;40(3):744-56 PMID: 11359579
  8. Cloning, nucleotide sequence, and regulation of katE encoding a sigma B-dependent catalase in Bacillus subtilis.
    J Bacteriol. 1995 Oct;177(19):5598-605 PMID: 7559348
  9. DNA microarray analysis of gene expression in response to physiological and genetic changes that affect tryptophan metabolism in Escherichia coli.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12170-5 PMID: 11027315
  10. Proteomics: a major new technology for the drug discovery process.
    Drug Discov Today. 1999 Feb;4(2):55-62 PMID: 10234157
  11. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis.
    Mol Microbiol. 1996 Jun;20(5):1083-91 PMID: 8809760
  12. YkdA and YvtA, HtrA-like serine proteases in Bacillus subtilis, engage in negative autoregulation and reciprocal cross-regulation of ykdA and yvtA gene expression.
    J Bacteriol. 2001 Jan;183(2):654-63 PMID: 11133960
  13. Real time quantitative PCR.
    Genome Res. 1996 Oct;6(10):986-94 PMID: 8908518
  14. The htpG gene of Bacillus subtilis belongs to class III heat shock genes and is under negative control.
    J Bacteriol. 1997 May;179(10):3103-9 PMID: 9150201
  15. Genome-wide analysis of the general stress response in Bacillus subtilis.
    Mol Microbiol. 2001 Aug;41(4):757-74 PMID: 11532142
  16. Exploring drug-induced alterations in gene expression in Mycobacterium tuberculosis by microarray hybridization.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12833-8 PMID: 10536008
  17. The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion.
    Mol Microbiol. 1997 Mar;23(5):921-33 PMID: 9076729
  18. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes.
    J Bacteriol. 1996 Feb;178(4):1088-93 PMID: 8576042
  19. Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance.
    Mol Microbiol. 1998 May;28(4):787-802 PMID: 9643546
  20. ScoC regulates peptide transport and sporulation initiation in Bacillus subtilis.
    J Bacteriol. 1999 Jul;181(13):4114-7 PMID: 10383984
  21. The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in gram-positive bacteria.
    Mol Microbiol. 1998 Nov;30(4):737-49 PMID: 10094622
  22. General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alkyl hydroperoxide reductase operon.
    J Bacteriol. 1996 Nov;178(22):6571-8 PMID: 8932314
  23. Harnessing the power of the genome in the search for new antibiotics.
    Science. 2000 Mar 17;287(5460):1973-6 PMID: 10720317
  24. Cloning, nucleotide sequence, and expression of the Bacillus subtilis lon gene.
    J Bacteriol. 1994 Nov;176(21):6518-27 PMID: 7961402
  25. A poly-gamma-glutamate synthetic system of Bacillus subtilis IFO 3336: gene cloning and biochemical analysis of poly-gamma-glutamate produced by Escherichia coli clone cells.
    Biochem Biophys Res Commun. 1999 Sep 16;263(1):6-12 PMID: 10486244
  26. Identification of a second oligopeptide transport system in Bacillus subtilis and determination of its role in sporulation.
    Mol Microbiol. 1994 Aug;13(3):417-26 PMID: 7997159
  27. Non-specific, general and multiple stress resistance of growth-restricted Bacillus subtilis cells by the expression of the sigmaB regulon.
    Mol Microbiol. 1998 Sep;29(5):1129-36 PMID: 9767581
  28. A novel spore peptidoglycan hydrolase of Bacillus cereus: biochemical characterization and nucleotide sequence of the corresponding gene, sleL.
    J Bacteriol. 2000 Mar;182(6):1499-506 PMID: 10692353
  29. Heat-shock and general stress response in Bacillus subtilis.
    Mol Microbiol. 1996 Feb;19(3):417-28 PMID: 8830234
  30. Cloning, sequencing, mapping, and transcriptional analysis of the groESL operon from Bacillus subtilis.
    J Bacteriol. 1992 Jun;174(12):3993-9 PMID: 1350777
  31. The yvaJ gene of Bacillus subtilis encodes a 3'-to-5' exoribonuclease and is not essential in a strain lacking polynucleotide phosphorylase.
    J Bacteriol. 2000 May;182(9):2639-42 PMID: 10762271
  32. Role of the transcriptional activator RocR in the arginine-degradation pathway of Bacillus subtilis.
    Mol Microbiol. 1997 May;24(4):825-37 PMID: 9194709
  33. A binding site for activation by the Bacillus subtilis AhrC protein, a repressor/activator of arginine metabolism.
    Mol Gen Genet. 1995 Aug 21;248(3):329-40 PMID: 7565595
  34. The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes.
    J Bacteriol. 1998 Dec;180(24):6681-8 PMID: 9852015
  35. Identification and transcriptional analysis of new members of the sigmaB regulon in Bacillus subtilis.
    Microbiology. 1999 Apr;145 ( Pt 4):869-80 PMID: 10220166
  36. Diagnosis of cellular states of microbial organisms using proteomics.
    Electrophoresis. 1999 Aug;20(11):2149-59 PMID: 10493120
  37. Molecular cloning and structure of the gene for esterase from a thermophilic bacterium, Bacillus stearothermophilus IFO 12550.
    Biosci Biotechnol Biochem. 1992 Dec;56(12):2074-5 PMID: 1369099
  38. Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis.
    Gene. 1996 Nov 28;181(1-2):77-83 PMID: 8973311
  39. First steps from a two-dimensional protein index towards a response-regulation map for Bacillus subtilis.
    Electrophoresis. 1997 Aug;18(8):1451-63 PMID: 9298659
  40. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis.
    J Bacteriol. 1994 Mar;176(5):1359-63 PMID: 8113175
  41. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis.
    J Bacteriol. 1998 Apr;180(7):1869-77 PMID: 9537387
  42. The sigma B-dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock.
    J Bacteriol. 1993 Apr;175(7):1929-35 PMID: 8458834
  43. A gene at 333 degrees on the Bacillus subtilis chromosome encodes the newly identified sigma B-dependent general stress protein GspA.
    J Bacteriol. 1995 Jun;177(12):3540-5 PMID: 7768864
  44. Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14674-9 PMID: 11121068
  45. Purification and initial characterization of AhrC: the regulator of arginine metabolism genes in Bacillus subtilis.
    Mol Microbiol. 1992 Jan;6(2):267-75 PMID: 1312212
  46. Cloning and characterization of the groESL operon from Bacillus subtilis.
    J Bacteriol. 1992 Jun;174(12):3981-92 PMID: 1350776
  47. The dnaK operon of Bacillus subtilis is heptacistronic.
    J Bacteriol. 1997 Feb;179(4):1153-64 PMID: 9023197
  48. The highly thermostable arginine repressor of Bacillus stearothermophilus: gene cloning and repressor-operator interactions.
    Mol Microbiol. 1997 Jul;25(2):385-98 PMID: 9282750
  49. Separate mechanisms activate sigma B of Bacillus subtilis in response to environmental and metabolic stresses.
    J Bacteriol. 1995 Jul;177(13):3771-80 PMID: 7601843
  50. Identification of target promoters for the Bacillus subtilis extracytoplasmic function sigma factor, sigma W.
    Mol Microbiol. 1999 Jan;31(1):361-71 PMID: 9987136
  51. Transcription of the nfrA-ywcH operon from Bacillus subtilis is specifically induced in response to heat.
    J Bacteriol. 2000 Aug;182(16):4384-93 PMID: 10913069
  52. Post-transcriptional regulation of the Bacillus subtilis dnaK operon.
    Mol Microbiol. 1999 Jun;32(6):1183-97 PMID: 10383760
  53. Operator interactions by the Bacillus subtilis arginine repressor/activator, AhrC: novel positioning and DNA-mediated assembly of a transcriptional activator at catabolic sites.
    Mol Microbiol. 1997 Oct;26(1):37-48 PMID: 9383188
  54. High-density microarray-mediated gene expression profiling of Escherichia coli.
    J Bacteriol. 2001 Jan;183(2):545-56 PMID: 11133948
  55. Ribosomes as sensors of heat and cold shock in Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5589-93 PMID: 2198567
  56. Escherichia coli proteome analysis using the gene-protein database.
    Electrophoresis. 1997 Aug;18(8):1243-51 PMID: 9298644
  57. Similar organization of the sigB and spoIIA operons encoding alternate sigma factors of Bacillus subtilis RNA polymerase.
    J Bacteriol. 1990 Oct;172(10):5575-85 PMID: 2170324
  58. The 2-oxoglutarate/malate translocator of chloroplast envelope membranes: molecular cloning of a transporter containing a 12-helix motif and expression of the functional protein in yeast cells.
    Biochemistry. 1995 Feb 28;34(8):2621-7 PMID: 7873543
  59. Analysis of the induction of general stress proteins of Bacillus subtilis.
    Microbiology. 1994 Apr;140 ( Pt 4):741-52 PMID: 8012595
  60. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria.
    Mol Microbiol. 1999 Jan;31(1):117-31 PMID: 9987115
  61. Bacillus subtilis YqkI is a novel malic/Na+-lactate antiporter that enhances growth on malate at low protonmotive force.
    J Biol Chem. 2000 Sep 29;275(39):30287-92 PMID: 10903309
  62. Identification of sigma(B)-dependent genes in Bacillus subtilis using a promoter consensus-directed search and oligonucleotide hybridization.
    J Bacteriol. 1999 Sep;181(18):5718-24 PMID: 10482513
  63. Sequences required for regulation of arginine biosynthesis promoters are conserved between Bacillus subtilis and Escherichia coli.
    Mol Microbiol. 1989 Jan;3(1):23-8 PMID: 2497296
  64. Expression of ykdA, encoding a Bacillus subtilis homologue of HtrA, is heat shock inducible and negatively autoregulated.
    J Bacteriol. 2000 Mar;182(6):1592-9 PMID: 10692364
  65. SubtiList: a relational database for the Bacillus subtilis genome.
    Microbiology. 1995 Feb;141 ( Pt 2):261-8 PMID: 7704253
  66. Mapping regulatory networks in microbial cells.
    Trends Microbiol. 1999 Aug;7(8):320-8 PMID: 10431205
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2001-12-00
Pages
7318-28
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC95581
Subset
IM
Analysis Services
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