Previous Article | Next Article 
Journal of Bacteriology, January 2003, p. 243-253, Vol. 185, No. 1
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.1.243-253.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
The Global Transcriptional Response of Bacillus subtilis to Peroxide Stress Is Coordinated by Three Transcription Factors
John D. Helmann,1* Ming Fang Winston Wu,2 Ahmed Gaballa,1 Phil A. Kobel,2,
Maud M. Morshedi,2 Paul Fawcett,3 and Chris Paddon2,
Department of Microbiology, Cornell University, Ithaca, New York 14853-8101,1
Affymax Research Institute, Santa Clara, California 95051,2
Department of Biochemistry, Stanford University School of Medicine, Stanford, California 943053
Received 5 August 2002/
Accepted 30 September 2002
Bacillus subtilis exhibits a complex adaptive response to low levels of peroxides. We used global transcriptional profiling to monitor the magnitude and kinetics of changes in the mRNA population after exposure to either hydrogen peroxide (H2O2) or tert-butyl peroxide (t-buOOH). The peroxide stimulons could be largely accounted for by three regulons controlled by the PerR,
B, and OhrR transcription factors. Three members of the PerR regulon (katA, mrgA, and zosA) were strongly induced by H2O2 and weakly induced by t-buOOH. The remaining members of the PerR regulon were only modestly up-regulated by peroxide treatment. Overall, the magnitude of peroxide induction of PerR regulon genes corresponded well with the extent of derepression in a perR mutant strain. The
B regulon was activated by 58 µM H2O2 but not by 8 µM H2O2 and was strongly activated by either t-buOOH or, in a control experiment, tert-butyl alcohol. Apart from the
B regulon there was a single gene, ohrA, that was strongly and rapidly induced by t-buOOH exposure. This gene, controlled by the peroxide-sensing repressor OhrR, was not induced by any of the other conditions tested.
* Corresponding author. Mailing address: Department of Microbiology, Cornell University, Ithaca, NY 14853-8101. Phone: (607) 255-6570. Fax: (607) 255-3904. E-mail:
jdh9{at}cornell.edu.
Present address: DiscoveRx, Fremont, CA 94538.
Present address: Xenoport, Inc., Santa Clara, CA 95051.
Journal of Bacteriology, January 2003, p. 243-253, Vol. 185, No. 1
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.1.243-253.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Reott, M. A., Parker, A. C., Rocha, E. R., Smith, C. J.
(2009). Thioredoxins in Redox Maintenance and Survival during Oxidative Stress of Bacteroides fragilis. J. Bacteriol.
191: 3384-3391
[Abstract]
[Full Text]
-
Ballal, A., Manna, A. C.
(2009). Regulation of Superoxide Dismutase (sod) Genes by SarA in Staphylococcus aureus. J. Bacteriol.
191: 3301-3310
[Abstract]
[Full Text]
-
Herve-Jimenez, L., Guillouard, I., Guedon, E., Boudebbouze, S., Hols, P., Monnet, V., Maguin, E., Rul, F.
(2009). Postgenomic Analysis of Streptococcus thermophilus Cocultivated in Milk with Lactobacillus delbrueckii subsp. bulgaricus: Involvement of Nitrogen, Purine, and Iron Metabolism. Appl. Environ. Microbiol.
75: 2062-2073
[Abstract]
[Full Text]
-
Hochgrafe, F., Wolf, C., Fuchs, S., Liebeke, M., Lalk, M., Engelmann, S., Hecker, M.
(2008). Nitric Oxide Stress Induces Different Responses but Mediates Comparable Protein Thiol Protection in Bacillus subtilis and Staphylococcus aureus. J. Bacteriol.
190: 4997-5008
[Abstract]
[Full Text]
-
Pulliainen, A. T., Hytonen, J., Haataja, S., Finne, J.
(2008). Deficiency of the Rgg Regulator Promotes H2O2 Resistance, AhpCF-Mediated H2O2 Decomposition, and Virulence in Streptococcus pyogenes. J. Bacteriol.
190: 3225-3235
[Abstract]
[Full Text]
-
Oh, S.-Y., Shin, J.-H., Roe, J.-H.
(2007). Dual Role of OhrR as a Repressor and an Activator in Response to Organic Hydroperoxides in Streptomyces coelicolor. J. Bacteriol.
189: 6284-6292
[Abstract]
[Full Text]
-
Mukhopadhyay, A., Redding, A. M., Joachimiak, M. P., Arkin, A. P., Borglin, S. E., Dehal, P. S., Chakraborty, R., Geller, J. T., Hazen, T. C., He, Q., Joyner, D. C., Martin, V. J. J., Wall, J. D., Yang, Z. K., Zhou, J., Keasling, J. D.
(2007). Cell-Wide Responses to Low-Oxygen Exposure in Desulfovibrio vulgaris Hildenborough. J. Bacteriol.
189: 5996-6010
[Abstract]
[Full Text]
-
Passalacqua, K. D., Bergman, N. H., Lee, J. Y., Sherman, D. H., Hanna, P. C.
(2007). The Global Transcriptional Responses of Bacillus anthracis Sterne (34F2) and a {Delta}sodA1 Mutant to Paraquat Reveal Metal Ion Homeostasis Imbalances during Endogenous Superoxide Stress. J. Bacteriol.
189: 3996-4013
[Abstract]
[Full Text]
-
Lee, J.-W., Soonsanga, S., Helmann, J. D.
(2007). A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. Proc. Natl. Acad. Sci. USA
104: 8743-8748
[Abstract]
[Full Text]
-
Leelakriangsak, M., Zuber, P.
(2007). Transcription from the P3 Promoter of the Bacillus subtilis spx Gene Is Induced in Response to Disulfide Stress. J. Bacteriol.
189: 1727-1735
[Abstract]
[Full Text]
-
Hyde, J. A., Seshu, J., Skare, J. T.
(2006). Transcriptional profiling of Borrelia burgdorferi containing a unique bosR allele identifies a putative oxidative stress regulon.. Microbiology
152: 2599-2609
[Abstract]
[Full Text]
-
Lee, J.-W., Helmann, J. D.
(2006). Biochemical Characterization of the Structural Zn2+ Site in the Bacillus subtilis Peroxide Sensor PerR. J. Biol. Chem.
281: 23567-23578
[Abstract]
[Full Text]
-
Seib, K. L., Wu, H.-J., Kidd, S. P., Apicella, M. A., Jennings, M. P., McEwan, A. G.
(2006). Defenses against Oxidative Stress in Neisseria gonorrhoeae: a System Tailored for a Challenging Environment. Microbiol. Mol. Biol. Rev.
70: 344-361
[Abstract]
[Full Text]
-
Even, S., Burguiere, P., Auger, S., Soutourina, O., Danchin, A., Martin-Verstraete, I.
(2006). Global Control of Cysteine Metabolism by CymR in Bacillus subtilis. J. Bacteriol.
188: 2184-2197
[Abstract]
[Full Text]
-
Maalej, S., Dammak, I., Dukan, S.
(2006). The impairment of superoxide dismutase coordinates the derepression of the PerR regulon in the response of Staphylococcus aureus to HOCl stress.. Microbiology
152: 855-861
[Abstract]
[Full Text]
-
Rea, R., Hill, C., Gahan, C. G. M.
(2005). Listeria monocytogenes PerR Mutants Display a Small-Colony Phenotype, Increased Sensitivity to Hydrogen Peroxide, and Significantly Reduced Murine Virulence. Appl. Environ. Microbiol.
71: 8314-8322
[Abstract]
[Full Text]
-
Verneuil, N., Rince, A., Sanguinetti, M., Posteraro, B., Fadda, G., Auffray, Y., Hartke, A., Giard, J.-C.
(2005). Contribution of a PerR-like regulator to the oxidative-stress response and virulence of Enterococcus faecalis. Microbiology
151: 3997-4004
[Abstract]
[Full Text]
-
Stork, T., Michel, K.-P., Pistorius, E. K., Dietz, K.-J.
(2005). Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot
56: 3193-3206
[Abstract]
[Full Text]
-
Au, N., Kuester-Schoeck, E., Mandava, V., Bothwell, L. E., Canny, S. P., Chachu, K., Colavito, S. A., Fuller, S. N., Groban, E. S., Hensley, L. A., O'Brien, T. C., Shah, A., Tierney, J. T., Tomm, L. L., O'Gara, T. M., Goranov, A. I., Grossman, A. D., Lovett, C. M.
(2005). Genetic Composition of the Bacillus subtilis SOS System. J. Bacteriol.
187: 7655-7666
[Abstract]
[Full Text]
-
Zeller, T., Moskvin, O. V., Li, K., Klug, G., Gomelsky, M.
(2005). Transcriptome and Physiological Responses to Hydrogen Peroxide of the Facultatively Phototrophic Bacterium Rhodobacter sphaeroides. J. Bacteriol.
187: 7232-7242
[Abstract]
[Full Text]
-
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
[Abstract]
[Full Text]
-
Cao, M., Moore, C. M., Helmann, J. D.
(2005). Bacillus subtilis Paraquat Resistance Is Directed by {sigma}M, an Extracytoplasmic Function Sigma Factor, and Is Conferred by YqjL and BcrC. J. Bacteriol.
187: 2948-2956
[Abstract]
[Full Text]
-
Caimano, M. J., Eggers, C. H., Hazlett, K. R. O., Radolf, J. D.
(2004). RpoS Is Not Central to the General Stress Response in Borrelia burgdorferi but Does Control Expression of One or More Essential Virulence Determinants. Infect. Immun.
72: 6433-6445
[Abstract]
[Full Text]
-
Moore, C. M., Nakano, M. M., Wang, T., Ye, R. W., Helmann, J. D.
(2004). Response of Bacillus subtilis to Nitric Oxide and the Nitrosating Agent Sodium Nitroprusside. J. Bacteriol.
186: 4655-4664
[Abstract]
[Full Text]
-
Li, H., Singh, A. K., McIntyre, L. M., Sherman, L. A.
(2004). Differential Gene Expression in Response to Hydrogen Peroxide and the Putative PerR Regulon of Synechocystis sp. Strain PCC 6803. J. Bacteriol.
186: 3331-3345
[Abstract]
[Full Text]
-
Rea, R. B., Gahan, C. G. M., Hill, C.
(2004). Disruption of Putative Regulatory Loci in Listeria monocytogenes Demonstrates a Significant Role for Fur and PerR in Virulence. Infect. Immun.
72: 717-727
[Abstract]
[Full Text]
-
Mostertz, J., Scharf, C., Hecker, M., Homuth, G.
(2004). Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology
150: 497-512
[Abstract]
[Full Text]
-
Nakano, S., Kuster-Schock, E., Grossman, A. D., 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
[Abstract]
[Full Text]
-
Fuangthong, M., Helmann, J. D.
(2003). Recognition of DNA by Three Ferric Uptake Regulator (Fur) Homologs in Bacillus subtilis. J. Bacteriol.
185: 6348-6357
[Abstract]
[Full Text]