Genome-wide identification of genes directly regulated by the pleiotropic transcription factor Spx in Bacillus subtilis

Nucleic Acids Research

Volumn 40, Issue 19, 2012, Pages 9571-9583

  Rochat, Tatiana ^a   Nicolas, Pierre ^b   Delumeau, Olivier ^a   Rabatinová, Alžbeta ^c   Korelusová, Jana ^c   Leduc, Aurélie ^b   Bessières, Philippe ^b   Dervyn, Etienne ^a   Krásný, Libor ^c   Noirot, Philippe ^a  

^a UMR1319 MICALIS   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

^c INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

DIAMIDE; NUCLEOTIDE; RNA POLYMERASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SPX; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENOME; BACTERIAL STRAIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC REGULATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; CONSENSUS SEQUENCE; DIAMIDE; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; PROMOTER REGIONS, GENETIC; REGULON; STRESS, PHYSIOLOGICAL; SULFHYDRYL REAGENTS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS;

EID: 84868101287     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks755     Document Type: Article

References (56)

1. Mostertz, J., Hochgrafe, F., Jurgen, B., Schweder, T. and Hecker, M. (2008) The role of thioredoxin TrxA in Bacillus subtilis: a proteomics and transcriptomics approach. Proteomics, 8, 2676-2690. (Pubitemid 351988572)
2. Scharf, C., Riethdorf, S., Ernst, H., Engelmann, S., Volker, U. and Hecker, M. (1998) Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J. Bacteriol., 180, 1869-1877. (Pubitemid 28173069)
3. Smits, W.K., Dubois, J.Y., Bron, S., van Dijl, J.M. and Kuipers, O.P. (2005) Tricksy business: transcriptome analysis reveals the involvement of thioredoxin A in redox homeostasis, oxidative stress, sulfur metabolism, and cellular differentiation in Bacillus subtilis. J. Bacteriol., 187, 3921-3930. (Pubitemid 40827775)
4. Nakano, S., Kuster-Schock, E., Grossman, A.D. and Zuber, P. (2003) Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc. Natl Acad. Sci. USA, 100, 13603-13608. (Pubitemid 37444787)
5. Duwat, P., Ehrlich, S.D. and Gruss, A. (1999) Effects of metabolic flux on stress response pathways in Lactococcus lactis. Mol. Microbiol., 31, 845-858. (Pubitemid 29057287)
6. Wang, C., Fan, J., Niu, C., Wang, C., Villaruz, A.E., Otto, M. and Gao, Q. (2010) Role of spx in biofilm formation of Staphylococcus epidermidis. FEMS Immunol. Med. Microbiol., 59, 152-160.
7. Kajfasz, J.K., Rivera-Ramos, I., Abranches, J., Martinez, A.R., Rosalen, P.L., Derr, A.M., Quivey, R.G. and Lemos, J.A. (2010) Two Spx proteins modulate stress tolerance, survival, and virulence in Streptococcus mutans. J. Bacteriol., 192, 2546-2556.
8. Turlan, C., Prudhomme, M., Fichant, G., Martin, B. and Gutierrez, C. (2009) SpxA1, a novel transcriptional regulator involved in X-state (competence) development in Streptococcus pneumoniae. Mol. Microbiol., 73, 492-506.
9. Pamp, S.J., Frees, D., Engelmann, S., Hecker, M. and Ingmer, H. (2006) Spx is a global effector impacting stress tolerance and biofilm formation in Staphylococcus aureus. J. Bacteriol., 188, 4861-4870. (Pubitemid 43956084)
10. Reder, A., Hoper, D., Weinberg, C., Gerth, U., Fraunholz, M. and Hecker, M. (2008) The Spx paralogue MgsR (YqgZ) controls a subregulon within the general stress response of Bacillus subtilis. Mol. Microbiol., 69, 1104-1120.
11. Reyes, D.Y. and Zuber, P. (2008) Activation of transcription initiation by Spx: formation of transcription complex and identification of a Cis-acting element required for transcriptional activation. Mol. Microbiol., 69, 765-779. (Pubitemid 351962568)
12. Antelmann, H., Scharf, C. and Hecker, M. (2000) Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J. Bacteriol., 182, 4478-4490. (Pubitemid 30599811)
13. Leelakriangsak, M., Kobayashi, K. and Zuber, P. (2007) Dual negative control of spx transcription initiation from the P3 promoter by repressors PerR and YodB in Bacillus subtilis. J. Bacteriol., 189, 1736-1744. (Pubitemid 46446136)
14. Zhang, Y. and Zuber, P. (2007) Requirement of the zinc-binding domain of ClpX for Spx proteolysis in Bacillus subtilis and effects of disulfide stress on ClpXP activity. J. Bacteriol., 189, 7669-7680. (Pubitemid 350035077)
15. Nakano, S., Erwin, K.N., Ralle, M. and Zuber, P. (2005) Redox-sensitive transcriptional control by a thiol/disulphide switch in the global regulator, Spx. Mol. Microbiol., 55, 498-510. (Pubitemid 40179383)
16. Leichert, L.I., Scharf, C. and Hecker, M. (2003) Global characterization of disulfide stress in Bacillus subtilis. J. Bacteriol., 185, 1967-1975. (Pubitemid 36297897)
17. Nakano, S., Nakano, M.M., Zhang, Y., Leelakriangsak, M. and Zuber, P. (2003) A regulatory protein that interferes with activator-stimulated transcription in bacteria. Proc. Natl Acad. Sci. USA, 100, 4233-4238. (Pubitemid 36418186)
18. Zhang, Y., Nakano, S., Choi, S.Y. and Zuber, P. (2006) Mutational analysis of the Bacillus subtilis RNA polymerase alpha C-terminal domain supports the interference model of Spx-dependent repression. J. Bacteriol., 188, 4300-4311. (Pubitemid 43865749)
19. Nakano, M.M., Lin, A., Zuber, C.S., Newberry, K.J., Brennan, R.G. and Zuber, P. (2010) Promoter recognition by a complex of Spx and the C-terminal domain of the RNA polymerase alpha subunit. PLoS One, 5, e8664.
20. Tam le, T., Antelmann, H., Eymann, C., Albrecht, D., Bernhardt, J. and Hecker, M. (2006) Proteome signatures for stress and starvation in Bacillus subtilis as revealed by a 2-D gel image color coding approach. Proteomics, 6, 4565-4585. (Pubitemid 44336972)
21. Leelakriangsak, M., Huyen, N.T., Towe, S., van Duy, N., Becher, D., Hecker, M., Antelmann, H. and Zuber, P. (2008) Regulation of quinone detoxification by the thiol stress sensing DUF24/MarR-like repressor, YodB in Bacillus subtilis. Mol. Microbiol., 67, 1108-1124. (Pubitemid 351207337)
22. Towe, S., Leelakriangsak, M., Kobayashi, K., Van Duy, N., Hecker, M., Zuber, P. and Antelmann, H. (2007) The MarR-type repressor MhqR (YkvE) regulates multiple dioxygenases/glyoxalases and an azoreductase which confer resistance to 2-methylhydroquinone and catechol in Bacillus subtilis. Mol. Microbiol., 66, 40-54. (Pubitemid 47414789)
23. Nguyen, T.T., Eiamphungporn, W., Mader, U., Liebeke, M., Lalk, M., Hecker, M., Helmann, J.D. and Antelmann, H. (2009) Genome-wide responses to carbonyl electrophiles in Bacillus subtilis: control of the thiol-dependent formaldehyde dehydrogenase AdhA and cysteine proteinase YraA by the MerR-family regulator YraB (AdhR). Mol. Microbiol., 71, 876-894.
24. Yurimoto, H., Hirai, R., Matsuno, N., Yasueda, H., Kato, N. and Sakai, Y. (2005) HxlR, a member of the DUF24 protein family, is a DNA-binding protein that acts as a positive regulator of the formaldehyde-inducible hxlAB operon in Bacillus subtilis. Mol. Microbiol., 57, 511-519. (Pubitemid 40979349)
25. Nicolas, P., Mäder, U., Dervyn, E., Rochat, T., Leduc, A., Pigeonneau, N., Bidnenko, E., Marchadier, E., Hoebeke, M., Aymerich, S. et al. (2012) Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science, 335, 1103-1106.
26. Buescher, J.M., Liebermeister, W., Jules, M., Uhr, M., Muntel, J., Botella, E., Hessling, B., Kleijn, R.J., Le Chat, L., Lecointe, F. et al. (2012) Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science, 335, 1099-1103.
27. Casadaban, M.J. and Cohen, S.N. (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol., 138, 179-207. (Pubitemid 10044378)
28. Zeghouf, M., Li, J., Butland, G., Borkowska, A., Canadien, V., Richards, D., Beattie, B., Emili, A. and Greenblatt, J.F. (2004) Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J. Proteome Res., 3, 463-468. (Pubitemid 39207350)
29. Rasmussen, S., Nielsen, H.B. and Jarmer, H. (2009) The transcriptionally active regions in the genome of Bacillus subtilis. Mol. Microbiol., 73, 1043-1057.
30. Reppas, N.B., Wade, J.T., Church, G.M. and Struhl, K. (2006) The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol. Cell, 24, 747-757. (Pubitemid 44839217)
31. Barbe, V., Cruveiller, S., Kunst, F., Lenoble, P., Meurice, G., Sekowska, A., Vallenet, D., Wang, T., Moszer, I., Medigue, C. et al. (2009) From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology, 155, 1758-1775.
32. Nicolas, P., Leduc, A., Robin, S., Rasmussen, S., Jarmer, H. and Bessieres, P. (2009) Transcriptional landscape estimation from tiling array data using a model of signal shift and drift. Bioinformatics, 25, 2341-2347.
33. Bolstad, B.M., Irizarry, R.A., Astrand, M. and Speed, T.P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 19, 185-193. (Pubitemid 36181903)
34. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., Bertero, M.G., Bessieres, P., Bolotin, A., Borchert, S. et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature, 390, 249-256. (Pubitemid 27513299)
35. Moszer, I., Jones, L.M., Moreira, S., Fabry, C. and Danchin, A. (2002) SubtiList: the reference database for the Bacillus subtilis genome. Nucleic Acids Res., 30, 62-65. (Pubitemid 34679505)
36. Delumeau, O., Lecointe, F., Muntel, J., Guillot, A., Guedon, E., Monnet, V., Hecker, M., Becher, D., Polard, P. and Noirot, P. (2011) The dynamic protein partnership of RNA polymerase in Bacillus subtilis. Proteomics, 11, 2992-3001.
37. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J. and Mann, M. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics, 4, 1265-1272. (Pubitemid 41448714)
38. Qi, Y. and Hulett, F.M. (1998) PhoP-P and RNA polymerase sigmaA holoenzyme are sufficient for transcription of Pho regulon promoters in Bacillus subtilis: PhoP-P activator sites within the coding region stimulate transcription in vitro. Mol. Microbiol., 28, 1187-1197. (Pubitemid 28293542)
39. Chang, B.Y. and Doi, R.H. (1990) Overproduction, purification, and characterization of Bacillus subtilis RNA polymerase sigma A factor. J. Bacteriol., 172, 3257-3263. (Pubitemid 20179781)
40. Juang, Y.L. and Helmann, J.D. (1994) A promoter melting region in the primary sigma factor of Bacillus subtilis. Identification of functionally important aromatic amino acids. J. Mol. Biol., 235, 1470-1488.
41. Sojka, L., Kouba, T., Barvik, I., Sanderova, H., Maderova, Z., Jonak, J. and Krasny, L. (2011) Rapid changes in gene expression: DNA determinants of promoter regulation by the concentration of the transcription initiating NTP in Bacillus subtilis. Nucleic Acids Res., 39, 4598-4611.
42. Ishikawa, S., Oshima, T., Kurokawa, K., Kusuya, Y. and Ogasawara, N. (2010) RNA polymerase trafficking in Bacillus subtilis cells. J. Bacteriol., 192, 5778-5787.
43. Kruger, E., Witt, E., Ohlmeier, S., Hanschke, R. and Hecker, M. (2000) The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J. Bacteriol., 182, 3259-3265. (Pubitemid 30326944)
44. Antelmann, H., Hecker, M. and Zuber, P. (2008) Proteomic signatures uncover thiol-specific electrophile resistance mechanisms in Bacillus subtilis. Expert Rev. Proteomics, 5, 77-90. (Pubitemid 351287743)
45. Chi, B.K., Gronau, K., Mader, U., Hessling, B., Becher, D. and Antelmann, H. (2011) S-bacillithiolation protects against hypochlorite stress in Bacillus subtilis as revealed by transcriptomics and redox proteomics. Mol. Cell. Proteomics, 10, M111 009506.
46. Zuber, P., Chauhan, S., Pilaka, P., Nakano, M.M., Gurumoorthy, S., Lin, A.A., Barendt, S.M., Chi, B.K., Antelmann, H. and Mader, U. (2011) Phenotype enhancement screen of a regulatory spx mutant unveils a role for the ytpQ gene in the control of iron homeostasis. PLoS One, 6, e25066.
47. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W. and Noble, W.S. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res., 37, W202-W208.
48. Helmann, J.D. (1995) Compilation and analysis of Bacillus subtilis sigma A-dependent promoter sequences: evidence for extended contact between RNA polymerase and upstream promoter DNA. Nucleic Acids Res., 23, 2351-2360.
49. Gaballa, A., Newton, G.L., Antelmann, H., Parsonage, D., Upton, H., Rawat, M., Claiborne, A., Fahey, R.C. and Helmann, J.D. (2010) Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in Bacilli. Proc. Natl Acad. Sci. USA, 107, 6482-6486.
50. Choi, S.Y., Reyes, D., Leelakriangsak, M. and Zuber, P. (2006) The global regulator Spx functions in the control of organosulfur metabolism in Bacillus subtilis. J. Bacteriol., 188, 5741-5751. (Pubitemid 44384082)
51. Burguiere, P., Auger, S., Hullo, M.F., Danchin, A. and Martin-Verstraete, I. (2004) Three different systems participate in L-cystine uptake in Bacillus subtilis. J. Bacteriol., 186, 4875-4884. (Pubitemid 38970814)
52. Even, S., Burguiere, P., Auger, S., Soutourina, O., Danchin, A. and Martin-Verstraete, I. (2006) Global control of cysteine metabolism by CymR in Bacillus subtilis. J. Bacteriol., 188, 2184-2197. (Pubitemid 43376472)
53. Kruger, E., Volker, U. and Hecker, M. (1994) Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J. Bacteriol., 176, 3360-3367. (Pubitemid 24166729)
54. Elsholz, A.K., Hempel, K., Pother, D.C., Becher, D., Hecker, M. and Gerth, U. (2011) CtsR inactivation during thiol-specific stress in low GC, Gram+bacteria. Mol. Microbiol., 79, 772-785.
55. Garg, S.K., Kommineni, S., Henslee, L., Zhang, Y. and Zuber, P. (2009) The YjbH protein of Bacillus subtilis enhances ClpXP-catalyzed proteolysis of Spx. J. Bacteriol., 191, 1268-1277.
56. Larsson, J.T., Rogstam, A. and von Wachenfeldt, C. (2007) YjbH is a novel negative effector of the disulphide stress regulator, Spx, in Bacillus subtilis. Mol. Microbiol., 66, 669-684. (Pubitemid 47621855)