Skip to main content
SpringerLink
Log in

Time-Related Transcriptome Analysis of B. subtilis 168 During Growth with Glucose

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Gene expression in Bacillus subtilis from late exponential to stationary phase was monitored by DNA microarrays with samples taken from the culture in LB broth with glucose supplement to prevent sporulation. Three major patterns of gene expression as revealed in this study were consistent to the expression profiling of PerR/Spx regulons and three major sigma factors—SigA, SigB, and SigW. Expression of most SigA-dependent house-keeping genes was significantly decreased and remained at low levels in the stationary phase. The sigB gene and additional genes of the SigB regulon for stress response exhibited a distinct pattern of transient induction with a peak in transition phase. The majority of induced genes after cessation of SigB-dependent surge were subjected to regulation by SigW, PerR, and Spx in response to oxidative stress. No induction of spo0A and skfA regulons supports the suppression of sporulation and cannibalism processes in the stationary phase by glucose supplement. In summary, these results depicted complicated strategies by cells to adapt changes from the fast growing exponential phase toward the stationary phase. The absence of programed cell death and sporulation greatly facilitated data analysis and the identification of distinct expression patterns in the stationary phase of growth in B. subtilis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Yoshimura M, Asai K, Sadaie Y, Yoshikawa H (2004) Interaction of Bacillus subtilis extracytoplasmic function (ECF) sigma factors with the N-terminal regions of their potential anti-sigma factors. Microbiology 150:591–599

    Article  CAS  PubMed  Google Scholar 

  2. Haldenwang WG (1995) The sigma factors of Bacillus subtilis. Microbiol Rev 59:1–30

    CAS  PubMed Central  PubMed  Google Scholar 

  3. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A et al (2012) Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335:1103–1106

    Article  CAS  PubMed  Google Scholar 

  4. Mäder UM, Antelmann HA, Buder TB, Dahl MD, Hecker MH et al (2002) Bacillus subtilis functional genomics: genome-wide analysis of the DegS-DegU regulon by transcriptomics and proteomics. Mol Genet Genomics 268:455–467

    Article  PubMed  Google Scholar 

  5. Blencke H-M, Homuth G, Ludwig H, Mader U, Hecker M et al (2003) Transcriptional profiling of gene expression in response to glucose in Bacillus subtilis: regulation of the central metabolic pathways. Metab Eng 5:133–149

    Article  CAS  PubMed  Google Scholar 

  6. Pietiäinen M, Gardemeister M, Mecklin M, Leskelä S, Sarvas M et al (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

    Article  PubMed  Google Scholar 

  7. Petersohn A, Brigulla M, Haas S, Hoheisel JD, Völker U et al (2001) Global analysis of the general stress response of Bacillus subtilis. J Bacteriol 183:5617–5631

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Blom E-J, Ridder ANJA, Lulko AT, Roerdink JBTM, Kuipers OP (2011) Time-resolved transcriptomics and bioinformatic analyses reveal intrinsic stress responses during batch culture of Bacillus subtilis. PLoS One 6:e27160

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Stephenson K, Harwood CR (1999) Cellular lysis in Bacillus subtilis; the affect of multiple extracellular protease deficiencies. Lett Appl Microbiol 29:141–145

    Article  CAS  Google Scholar 

  10. Vitikainen M, Lappalainen I, Seppala R, Antelmann H, Boer H et al (2004) Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J Biol Chem 279:19302–19314

    Article  CAS  PubMed  Google Scholar 

  11. Yang C-K, Ewis H, Zhang X-Z, Lu C-D, Hu HJ et al (2011) Nonclassical protein secretion by Bacillus subtilis in the stationary phase is not due to cell lysis. J Bacteriol 193:5607–5615

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Kwon DH, Lu C-D (2006) Polyamines induce resistance to cationic peptide, aminoglycoside, and quinolone antibiotics in Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother 50:1615–1622

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Lu C-D, Yang Z, Li W (2004) Transcriptome analysis of the ArgR regulon in Pseudomonas aeruginosa. J Bacteriol 186:3855–3861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Jarmer H, Larsen TS, Krogh A, Saxild HH, Brunak S et al (2001) Sigma A recognition sites in the Bacillus subtilis genome. Microbiology 147:2417–2424

    CAS  PubMed  Google Scholar 

  15. Sierro N, Makita Y, de Hoon M, Nakai K (2008) DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res 36:D93–D96

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Holtmann G, Brigulla M, Steil L, Schütz A, Barnekow K et al (2004) RsbV-independent induction of the SigB-dependent general stress regulon of Bacillus subtilis during growth at high temperature. J Bacteriol 186:6150–6158

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Zhang S, Haldenwang WG (2003) RelA is a component of the nutritional stress activation pathway of the Bacillus subtilis transcription factor sigmaB. J Bacteriol 185:5714–5721

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Kuo S, Zhang S, Woodbury RL, Haldenwang WG (2004) Associations between Bacillus subtilis σB regulators in cell extracts. Microbiology 150:4125–4136

    Article  CAS  PubMed  Google Scholar 

  19. Brigulla M, Hoffmann T, Krisp A, Volker A, Bremer E et al (2003) Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J Bacteriol 185:4305–4314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Akbar S, Gaidenko TA, Kang CM, O’Reilly M, Devine KM et al (2001) New family of regulators in the environmental signaling pathway which activates the general stress transcription factor sigmaB of Bacillus subtilis. J Bacteriol 183:1329–1338

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Pané-Farré J, Lewis R, Stülke J (2005) The RsbRST stress module in bacteria: a signalling system that may interact with different output modules. J Mol Microbiol Biotechnol 9:65–76

    Article  PubMed  Google Scholar 

  22. Zuber P (2009) Management of oxidative stress in Bacillus. Annu Rev Microbiol 63:575–597

    Article  CAS  PubMed  Google Scholar 

  23. Nannapaneni P, Hertwig F, Depke M, Hecker M, Mäder U et al (2012) Defining the structure of the general stress regulon of Bacillus subtilis using targeted microarray analysis and random forest classification. Microbiology 158:696–707

    Article  CAS  PubMed  Google Scholar 

  24. Fouet A, Namy O, Lambert G (2000) Characterization of the operon encoding the alternative ςB factor from Bacillus anthracis and its role in virulence. J Bacteriol 182:5036–5045

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Wise AA, Price CW (1995) 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 177:123–133

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G et al (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249–256

    Article  CAS  PubMed  Google Scholar 

  27. Voelker U, Voelker A, Maul B, Hecker M, Dufour A et al (1995) Separate mechanisms activate sigma B of Bacillus subtilis in response to environmental and metabolic stresses. J Bacteriol 177:3771–3780

    CAS  PubMed Central  PubMed  Google Scholar 

  28. Zhang S, Haldenwang WG (2005) Contributions of ATP, GTP, and redox state to nutritional stress activation of the Bacillus subtilis sigmaB transcription factor. J Bacteriol 187:7554–7560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Turner MS, Helmann JD (2000) Mutations in multidrug efflux homologs, sugar isomerases, and antimicrobial biosynthesis genes differentially elevate activity of the sigma X and sigma W factors in Bacillus subtilis. J Bacteriol 182:5202–5210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Cao M, Wang T, Ye R, Helmann JD (2002) Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis σW and σM regulons. Mol Microbiol 45:1267–1276

    Article  CAS  PubMed  Google Scholar 

  31. Kingston AW, Subramanian C, Rock CO, Helmann JD (2011) A σW-dependent stress response in Bacillus subtilis that reduces membrane fluidity. Mol Microbiol 81:69–79

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Ellermeier CD, Losick R (2006) Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis. Genes Dev 20:1911–1922

    Article  CAS  PubMed  Google Scholar 

  33. Yano K, Inoue H, Mori H, Yee LM, Matsuoka S et al (2011) Heterologous expression of the Oceanobacillus iheyensis SigW and its anti-protein RsiW in Bacillus subtilis. Biosci Biotechnol Biochem 75:966–975

    Article  CAS  PubMed  Google Scholar 

  34. Butcher BG, Helmann JD (2006) Identification of Bacillus subtilis σW-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol Microbiol 60:765–782

    Article  CAS  PubMed  Google Scholar 

  35. Stragier P (2006) To kill but not be killed: a delicate balance. Cell 124:461–463

    Article  CAS  PubMed  Google Scholar 

  36. Klimecka MM, Chruszcz M, Font J, Skarina T, Shumilin I et al (2011) Structural analysis of a putative aminoglycoside N-acetyltransferase from Bacillus anthracis. J Mol Biol 410:411–423

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S et al (2011) A widespread family of bacterial cell wall assembly proteins. EMBO J 30(24):4931–4941

    Article  CAS  PubMed  Google Scholar 

  38. Salzberg LI, Helmann JD (2007) An antibiotic-inducible cell wall-associated protein that protects Bacillus subtilis from autolysis. J Bacteriol 189:4671–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Rochat T, Nicolas P, Delumeau O, Rabatinová A, Korelusová J et al (2012) Genome-wide identification of genes directly regulated by the pleiotropic transcription factor Spx in Bacillus subtilis. Nucleic Acids Res 40:9571–9583

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Hayashi K, Ohsawa T, Kobayashi K, Ogasawara N, Ogura M (2005) The H2O2 stress-responsive regulator PerR positively regulates srfA expression in Bacillus subtilis. J Bacteriol 187:6659–6667

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Fuangthong M, Herbig AF, Bsat N, Helmann JD (2002) Regulation of the Bacillus subtilis fur and perR Genes by PerR: not all members of the PerR regulon are peroxide inducible. J Bacteriol 184:3276–3286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Zuber P (2004) Spx-RNA polymerase interaction and global transcriptional control during oxidative stress. J Bacteriol 186:1911–1918

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Antelmann H, Scharf C, Hecker M (2000) Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J Bacteriol 182:4478–4490

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Allenby NEE, O’Connor N, Prágai Z, Carter NM, Miethke M et al (2004) Post-transcriptional regulation of the Bacillus subtilis pst operon encoding a phosphate-specific ABC transporter. Microbiology 150:2619–2628

    Article  CAS  PubMed  Google Scholar 

  45. González-Pastor JE, Hobbs EC, Losick R (2003) Cannibalism by sporulating bacteria. Science 301:510–513

    Article  PubMed  Google Scholar 

  46. González-Pastor JE (2011) Cannibalism: a social behavior in sporulating Bacillus subtilis. FEMS Microbiol Rev 35:415–424

    Article  PubMed  Google Scholar 

  47. López D, Vlamakis H, Losick R, Kolter R (2009) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74:609–618

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a NIH research grant GM 34766. We thank Dr. Hsiuchin Yang for discussions and Sonja Young for the Microarray service in the GSU Biology Core Facility which is supported by the Georgia Research Alliance, Molecular Basis of Disease Program and Center for Biotechnology and Drug Design. CKY was the fellow of the Program in Molecular Basis of Diseases at Georgia State University.

Author information

Authors and Affiliations

  1. Department of Biology, Georgia State University, 161 Jesse Hill Drive, Atlanta, GA, 30303, USA

    Chun-Kai Yang, Phang C. Tai & Chung-Dar Lu

Authors
  1. Chun-Kai Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phang C. Tai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chung-Dar Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chung-Dar Lu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 35 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, CK., Tai, P.C. & Lu, CD. Time-Related Transcriptome Analysis of B. subtilis 168 During Growth with Glucose. Curr Microbiol 68, 12–20 (2014). https://doi.org/10.1007/s00284-013-0432-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-013-0432-4

Keywords

Search

Navigation