Previous Article | Next Article 
Journal of Bacteriology, December 1998, p. 6082-6089, Vol. 180, No. 23
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
The Staphylococcus aureus Alternative
Sigma Factor
B Controls the Environmental Stress
Response but Not Starvation Survival or Pathogenicity in a
Mouse Abscess Model
Pan F.
Chan,1
Simon J.
Foster,1,*
Eileen
Ingham,2 and
Mark O.
Clements1
Department of Molecular Biology and
Biotechnology, University of Sheffield, Western Bank, Sheffield, S10
2TN,1 and
Department of Microbiology,
University of Leeds, Leeds, LS2 9JT,2 United
Kingdom
Received 13 July 1998/Accepted 18 September 1998
The role of
B, an alternative sigma factor of
Staphylococcus aureus, has been characterized in response
to environmental stress, starvation-survival and recovery, and
pathogenicity.
B was mainly expressed during the
stationary phase of growth and was repressed by 1 M sodium chloride. A
sigB insertionally inactivated mutant was created. In
stress resistance studies,
B was shown to be involved in
recovery from heat shock at 54°C and in acid and hydrogen peroxide
resistance but not in resistance to ethanol or osmotic shock.
Interestingly, S. aureus acquired increased acid resistance
when preincubated at a sublethal pH 4 prior to exposure to a lethal pH
2. This acid-adaptive response resulting in tolerance was mediated via
sigB. However,
B was not vital for the
starvation-survival or recovery mechanisms.
B does not
have a major role in the expression of the global regulator of
virulence determinant biosynthesis, staphylococcal accessory regulator
(sarA), the production of a number of representative virulence factors, and pathogenicity in a mouse subcutaneous abscess model. However, SarA upregulates sigB expression in a
growth-phase-dependent manner. Thus,
B expression is
linked to the processes controlling virulence determinant production.
The role of
B as a major regulator of the stress
response, but not of starvation-survival, is discussed.
*
Corresponding author. Mailing address: Department of
Molecular Biology and Biotechnology, University of Sheffield, Firth
Court, Western Bank, Sheffield, S10 2TN, United Kingdom. Phone:
44-114-2224411. Fax: 44-114-2728697. E-mail:
s.foster{at}sheffield.ac.uk.
Journal of Bacteriology, December 1998, p. 6082-6089, Vol. 180, No. 23
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Schulthess, B., Meier, S., Homerova, D., Goerke, C., Wolz, C., Kormanec, J., Berger-Bachi, B., Bischoff, M.
(2009). Functional Characterization of the {sigma}B-Dependent yabJ-spoVG Operon in Staphylococcus aureus: Role in Methicillin and Glycopeptide Resistance. Antimicrob. Agents Chemother.
53: 1832-1839
[Abstract]
[Full Text]
-
Abram, F., Starr, E., Karatzas, K. A. G., Matlawska-Wasowska, K., Boyd, A., Wiedmann, M., Boor, K. J., Connally, D., O'Byrne, C. P.
(2008). Identification of Components of the Sigma B Regulon in Listeria monocytogenes That Contribute to Acid and Salt Tolerance. Appl. Environ. Microbiol.
74: 6848-6858
[Abstract]
[Full Text]
-
Ding, Y., Onodera, Y., Lee, J. C., Hooper, D. C.
(2008). NorB, an Efflux Pump in Staphylococcus aureus Strain MW2, Contributes to Bacterial Fitness in Abscesses. J. Bacteriol.
190: 7123-7129
[Abstract]
[Full Text]
-
Steidl, R., Pearson, S., Stephenson, R. E., Ledala, N., Sitthisak, S., Wilkinson, B. J., Jayaswal, R. K.
(2008). Staphylococcus aureus Cell Wall Stress Stimulon Gene-lacZ Fusion Strains: Potential for Use in Screening for Cell Wall-Active Antimicrobials. Antimicrob. Agents Chemother.
52: 2923-2925
[Abstract]
[Full Text]
-
Sowell, S. M., Norbeck, A. D., Lipton, M. S., Nicora, C. D., Callister, S. J., Smith, R. D., Barofsky, D. F., Giovannoni, S. J.
(2008). Proteomic Analysis of Stationary Phase in the Marine Bacterium "Candidatus Pelagibacter ubique". Appl. Environ. Microbiol.
74: 4091-4100
[Abstract]
[Full Text]
-
Haenni, M., Moreillon, P., Lazarevic, V.
(2007). Promoter and Transcription Analysis of Penicillin-Binding Protein Genes in Streptococcus gordonii. Antimicrob. Agents Chemother.
51: 2774-2783
[Abstract]
[Full Text]
-
Valle, J., Vergara-Irigaray, M., Merino, N., Penades, J. R., Lasa, I.
(2007). {sigma}B Regulates IS256-Mediated Staphylococcus aureus Biofilm Phenotypic Variation. J. Bacteriol.
189: 2886-2896
[Abstract]
[Full Text]
-
Oscarsson, J., Kanth, A., Tegmark-Wisell, K., Arvidson, S.
(2006). SarA Is a Repressor of hla ({alpha}-Hemolysin) Transcription in Staphylococcus aureus: Its Apparent Role as an Activator of hla in the Prototype Strain NCTC 8325 Depends on Reduced Expression of sarS. J. Bacteriol.
188: 8526-8533
[Abstract]
[Full Text]
-
Chaturongakul, S., Boor, K. J.
(2006). {sigma}B Activation under Environmental and Energy Stress Conditions in Listeria monocytogenes. Appl. Environ. Microbiol.
72: 5197-5203
[Abstract]
[Full Text]
-
Chatterjee, I., Somerville, G. A., Heilmann, C., Sahl, H.-G., Maurer, H. H., Herrmann, M.
(2006). Very Low Ethanol Concentrations Affect the Viability and Growth Recovery in Post-Stationary-Phase Staphylococcus aureus Populations. Appl. Environ. Microbiol.
72: 2627-2636
[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]
-
Schwan, W. R., Lehmann, L., McCormick, J.
(2006). Transcriptional Activation of the Staphylococcus aureus putP Gene by Low-Proline-High Osmotic Conditions and during Infection of Murine and Human Tissues. Infect. Immun.
74: 399-409
[Abstract]
[Full Text]
-
Kazmierczak, M. J., Wiedmann, M., Boor, K. J.
(2005). Alternative Sigma Factors and Their Roles in Bacterial Virulence. Microbiol. Mol. Biol. Rev.
69: 527-543
[Abstract]
[Full Text]
-
Senn, M. M., Giachino, P., Homerova, D., Steinhuber, A., Strassner, J., Kormanec, J., Fluckiger, U., Berger-Bachi, B., Bischoff, M.
(2005). Molecular Analysis and Organization of the {sigma}B Operon in Staphylococcus aureus. J. Bacteriol.
187: 8006-8019
[Abstract]
[Full Text]
-
Chatterjee, I., Becker, P., Grundmeier, M., Bischoff, M., Somerville, G. A., Peters, G., Sinha, B., Harraghy, N., Proctor, R. A., Herrmann, M.
(2005). Staphylococcus aureus ClpC Is Required for Stress Resistance, Aconitase Activity, Growth Recovery, and Death. J. Bacteriol.
187: 4488-4496
[Abstract]
[Full Text]
-
Streker, K., Freiberg, C., Labischinski, H., Hacker, J., Ohlsen, K.
(2005). Staphylococcus aureus NfrA (SA0367) Is a Flavin Mononucleotide-Dependent NADPH Oxidase Involved in Oxidative Stress Response. J. Bacteriol.
187: 2249-2256
[Abstract]
[Full Text]
-
Entenza, J.-M., Moreillon, P., Senn, M. M., Kormanec, J., Dunman, P. M., Berger-Bachi, B., Projan, S., Bischoff, M.
(2005). Role of {sigma}B in the Expression of Staphylococcus aureus Cell Wall Adhesins ClfA and FnbA and Contribution to Infectivity in a Rat Model of Experimental Endocarditis. Infect. Immun.
73: 990-998
[Abstract]
[Full Text]
-
Wright, J. S. III, Jin, R., Novick, R. P.
(2005). Transient interference with staphylococcal quorum sensing blocks abscess formation. Proc. Natl. Acad. Sci. USA
102: 1691-1696
[Abstract]
[Full Text]
-
Rigoulay, C., Entenza, J. M., Halpern, D., Widmer, E., Moreillon, P., Poquet, I., Gruss, A.
(2005). Comparative Analysis of the Roles of HtrA-Like Surface Proteases in Two Virulent Staphylococcus aureus Strains. Infect. Immun.
73: 563-572
[Abstract]
[Full Text]
-
Weinrick, B., Dunman, P. M., McAleese, F., Murphy, E., Projan, S. J., Fang, Y., Novick, R. P.
(2004). Effect of Mild Acid on Gene Expression in Staphylococcus aureus. J. Bacteriol.
186: 8407-8423
[Abstract]
[Full Text]
-
Chaussee, M. A., Callegari, E. A., Chaussee, M. S.
(2004). Rgg Regulates Growth Phase-Dependent Expression of Proteins Associated with Secondary Metabolism and Stress in Streptococcus pyogenes. J. Bacteriol.
186: 7091-7099
[Abstract]
[Full Text]
-
Jonsson, I.-M., Arvidson, S., Foster, S., Tarkowski, A.
(2004). Sigma Factor B and RsbU Are Required for Virulence in Staphylococcus aureus-Induced Arthritis and Sepsis. Infect. Immun.
72: 6106-6111
[Abstract]
[Full Text]
-
Pechous, R., Ledala, N., Wilkinson, B. J., Jayaswal, R. K.
(2004). Regulation of the Expression of Cell Wall Stress Stimulon Member Gene msrA1 in Methicillin-Susceptible or -Resistant Staphylococcus aureus. Antimicrob. Agents Chemother.
48: 3057-3063
[Abstract]
[Full Text]
-
Beenken, K. E., Dunman, P. M., McAleese, F., Macapagal, D., Murphy, E., Projan, S. J., Blevins, J. S., Smeltzer, M. S.
(2004). Global Gene Expression in Staphylococcus aureus Biofilms. J. Bacteriol.
186: 4665-4684
[Abstract]
[Full Text]
-
Bischoff, M., Dunman, P., Kormanec, J., Macapagal, D., Murphy, E., Mounts, W., Berger-Bachi, B., Projan, S.
(2004). Microarray-Based Analysis of the Staphylococcus aureus {sigma}B Regulon. J. Bacteriol.
186: 4085-4099
[Abstract]
[Full Text]
-
Makris, G., Wright, J. D., Ingham, E., Holland, K. T.
(2004). The hyaluronate lyase of Staphylococcus aureus - a virulence factor?. Microbiology
150: 2005-2013
[Abstract]
[Full Text]
-
Lithgow, J. K., Hayhurst, E. J., Cohen, G., Aharonowitz, Y., Foster, S. J.
(2004). Role of a Cysteine Synthase in Staphylococcus aureus. J. Bacteriol.
186: 1579-1590
[Abstract]
[Full Text]
-
Lithgow, J. K., Ingham, E., Foster, S. J.
(2004). Role of the hprT-ftsH locus in Staphylococcus aureus. Microbiology
150: 373-381
[Abstract]
[Full Text]
-
van Schaik, W., Tempelaars, M. H., Wouters, J. A., de Vos, W. M., Abee, T.
(2004). The Alternative Sigma Factor {sigma}B of Bacillus cereus: Response to Stress and Role in Heat Adaptation. J. Bacteriol.
186: 316-325
[Abstract]
[Full Text]
-
Uziel, O., Borovok, I., Schreiber, R., Cohen, G., Aharonowitz, Y.
(2004). Transcriptional Regulation of the Staphylococcus aureus Thioredoxin and Thioredoxin Reductase Genes in Response to Oxygen and Disulfide Stress. J. Bacteriol.
186: 326-334
[Abstract]
[Full Text]
-
Shaw, L., Golonka, E., Potempa, J., Foster, S. J.
(2004). The role and regulation of the extracellular proteases of Staphylococcus aureus. Microbiology
150: 217-228
[Abstract]
[Full Text]
-
Kazmierczak, M. J., Mithoe, S. C., Boor, K. J., Wiedmann, M.
(2003). Listeria monocytogenes {sigma}B Regulates Stress Response and Virulence Functions. J. Bacteriol.
185: 5722-5734
[Abstract]
[Full Text]
-
Novick, R. P., Jiang, D.
(2003). The staphylococcal saeRS system coordinates environmental signals with agr quorum sensing. Microbiology
149: 2709-2717
[Abstract]
[Full Text]
-
Karavolos, M. H., Horsburgh, M. J., Ingham, E., Foster, S. J.
(2003). Role and regulation of the superoxide dismutases of Staphylococcus aureus. Microbiology
149: 2749-2758
[Abstract]
[Full Text]
-
Cotter, P. D., Hill, C.
(2003). Surviving the Acid Test: Responses of Gram-Positive Bacteria to Low pH. Microbiol. Mol. Biol. Rev.
67: 429-453
[Abstract]
[Full Text]
-
Ferreira, A., Sue, D., O'Byrne, C. P., Boor, K. J.
(2003). Role of Listeria monocytogenes{sigma}B in Survival of Lethal Acidic Conditions and in the Acquired Acid Tolerance Response. Appl. Environ. Microbiol.
69: 2692-2698
[Abstract]
[Full Text]
-
Ando, M., Manabe, Y. C., Converse, P. J., Miyazaki, E., Harrison, R., Murphy, J. R., Bishai, W. R.
(2003). Characterization of the Role of the Divalent Metal Ion-Dependent Transcriptional Repressor MntR in the Virulence of Staphylococcus aureus. Infect. Immun.
71: 2584-2590
[Abstract]
[Full Text]
-
Sifri, C. D., Begun, J., Ausubel, F. M., Calderwood, S. B.
(2003). Caenorhabditis elegans as a Model Host for Staphylococcus aureus Pathogenesis. Infect. Immun.
71: 2208-2217
[Abstract]
[Full Text]
-
McAleese, F. M., Foster, T. J.
(2003). Analysis of mutations in the Staphylococcus aureus clfB promoter leading to increased expression. Microbiology
149: 99-109
[Abstract]
[Full Text]
-
Clarke, S. R., Harris, L. G., Richards, R. G., Foster, S. J.
(2002). Analysis of Ebh, a 1.1-Megadalton Cell Wall-Associated Fibronectin-Binding Protein of Staphylococcus aureus. Infect. Immun.
70: 6680-6687
[Abstract]
[Full Text]
-
Price, C. T. D., Singh, V. K., Jayaswal, R. K., Wilkinson, B. J., Gustafson, J. E.
(2002). Pine Oil Cleaner-Resistant Staphylococcus aureus: Reduced Susceptibility to Vancomycin and Oxacillin and Involvement of SigB. Appl. Environ. Microbiol.
68: 5417-5421
[Abstract]
[Full Text]
-
Horsburgh, M. J., Aish, J. L., White, I. J., Shaw, L., Lithgow, J. K., Foster, S. J.
(2002). {sigma}B Modulates Virulence Determinant Expression and Stress Resistance: Characterization of a Functional rsbU Strain Derived from Staphylococcus aureus 8325-4. J. Bacteriol.
184: 5457-5467
[Abstract]
[Full Text]
-
Periago, P. M., van Schaik, W., Abee, T., Wouters, J. A.
(2002). Identification of Proteins Involved in the Heat Stress Response of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol.
68: 3486-3495
[Abstract]
[Full Text]
-
Vilhelmsson, O., Miller, K. J.
(2002). Synthesis of Pyruvate Dehydrogenase in Staphylococcus aureus Is Stimulated by Osmotic Stress. Appl. Environ. Microbiol.
68: 2353-2358
[Abstract]
[Full Text]
-
Palma, M., Cheung, A. L.
(2001). sigma B Activity in Staphylococcus aureus Is Controlled by RsbU and an Additional Factor(s) during Bacterial Growth. Infect. Immun.
69: 7858-7865
[Abstract]
[Full Text]
-
Kies, S., Otto, M., Vuong, C., Gotz, F.
(2001). Identification of the sigB Operon in Staphylococcus epidermidis: Construction and Characterization of a sigB Deletion Mutant. Infect. Immun.
69: 7933-7936
[Abstract]
[Full Text]
-
Singh, V. K., Moskovitz, J., Wilkinson, B. J., Jayaswal, R. K.
(2001). Molecular characterization of a chromosomal locus in Staphylococcus aureus that contributes to oxidative defence and is highly induced by the cell-wall-active antibiotic oxacillin. Microbiology
147: 3037-3045
[Abstract]
[Full Text]
-
Ferreira, A., O'Byrne, C. P., Boor, K. J.
(2001). Role of {sigma}B in Heat, Ethanol, Acid, and Oxidative Stress Resistance and during Carbon Starvation in Listeria monocytogenes. Appl. Environ. Microbiol.
67: 4454-4457
[Abstract]
[Full Text]
-
Bischoff, M., Entenza, J. M., Giachino, P.
(2001). Influence of a Functional sigB Operon on the Global Regulators sar and agr in Staphylococcus aureus. J. Bacteriol.
183: 5171-5179
[Abstract]
[Full Text]
-
Schmidt, K. A., Manna, A. C., Gill, S., Cheung, A. L.
(2001). SarT, a Repressor of {alpha}-Hemolysin in Staphylococcus aureus. Infect. Immun.
69: 4749-4758
[Abstract]
[Full Text]
-
Wiltshire, M. D., Foster, S. J.
(2001). Identification and Analysis of Staphylococcus aureus Components Expressed by a Model System of Growth in Serum. Infect. Immun.
69: 5198-5202
[Abstract]
[Full Text]
-
Herbert, K. C., Foster, S. J.
(2001). Starvation survival in Listeria monocytogenes: characterization of the response and the role of known and novel components. Microbiology
147: 2275-2284
[Abstract]
[Full Text]
-
Horsburgh, M. J., Clements, M. O., Crossley, H., Ingham, E., Foster, S. J.
(2001). PerR Controls Oxidative Stress Resistance and Iron Storage Proteins and Is Required for Virulence in Staphylococcus aureus. Infect. Immun.
69: 3744-3754
[Abstract]
[Full Text]
-
Lindsay, J. A., Foster, S. J.
(2001). zur: a Zn2+-responsive regulatory element of Staphylococcus aureus. Microbiology
147: 1259-1266
[Abstract]
[Full Text]
-
Knobloch, J. K.-M., Bartscht, K., Sabottke, A., Rohde, H., Feucht, H.-H., Mack, D.
(2001). Biofilm Formation by Staphylococcus epidermidis Depends on Functional RsbU, an Activator of the sigB Operon: Differential Activation Mechanisms Due to Ethanol and Salt Stress. J. Bacteriol.
183: 2624-2633
[Abstract]
[Full Text]
-
Giachino, P., Engelmann, S., Bischoff, M.
(2001). {sigma}B Activity Depends on RsbU in Staphylococcus aureus. J. Bacteriol.
183: 1843-1852
[Abstract]
[Full Text]
-
Yarwood, J. M., McCormick, J. K., Schlievert, P. M.
(2001). Identification of a Novel Two-Component Regulatory System That Acts in Global Regulation of Virulence Factors of Staphylococcus aureus. J. Bacteriol.
183: 1113-1123
[Abstract]
[Full Text]
-
Chaussee, M. S., Watson, R. O., Smoot, J. C., Musser, J. M.
(2001). Identification of Rgg-Regulated Exoproteins of Streptococcus pyogenes. Infect. Immun.
69: 822-831
[Abstract]
[Full Text]
-
Gertz, S., Engelmann, S., Schmid, R., Ziebandt, A.-K., Tischer, K., Scharf, C., Hacker, J., Hecker, M.
(2000). Characterization of the sigma B Regulon in Staphylococcus aureus. J. Bacteriol.
182: 6983-6991
[Abstract]
[Full Text]
-
Chen, P., Ruiz, R. E., Li, Q., Silver, R. F., Bishai, W. R.
(2000). Construction and Characterization of a Mycobacterium tuberculosis Mutant Lacking the Alternate Sigma Factor Gene, sigF. Infect. Immun.
68: 5575-5580
[Abstract]
[Full Text]
-
King, K. Y., Horenstein, J. A., Caparon, M. G.
(2000). Aerotolerance and Peroxide Resistance in Peroxidase and PerR Mutants of Streptococcus pyogenes. J. Bacteriol.
182: 5290-5299
[Abstract]
[Full Text]
-
Fouet, A., Namy, O., Lambert, G.
(2000). Characterization of the Operon Encoding the Alternative sigma B Factor from Bacillus anthracis and Its Role in Virulence. J. Bacteriol.
182: 5036-5045
[Abstract]
[Full Text]
-
Nicholas, R. O., Li, T., McDevitt, D., Marra, A., Sucoloski, S., Demarsh, P. L., Gentry, D. R.
(1999). Isolation and Characterization of a sigB Deletion Mutant of Staphylococcus aureus. Infect. Immun.
67: 3667-3669
[Abstract]
[Full Text]
-
Clements, M. O., Watson, S. P., Foster, S. J.
(1999). Characterization of the Major Superoxide Dismutase of Staphylococcus aureus and Its Role in Starvation Survival, Stress Resistance, and Pathogenicity. J. Bacteriol.
181: 3898-3903
[Abstract]
[Full Text]
-
Völker, U., Maul, B., Hecker, M.
(1999). Expression of the sigma B-Dependent General Stress Regulon Confers Multiple Stress Resistance in Bacillus subtilis. J. Bacteriol.
181: 3942-3948
[Abstract]
[Full Text]
-
Miyazaki, E., Chen, J.-M., Ko, C., Bishai, W. R.
(1999). The Staphylococcus aureus rsbW (orf159) Gene Encodes an Anti-Sigma Factor of SigB. J. Bacteriol.
181: 2846-2851
[Abstract]
[Full Text]
-
Clements, M. O., Watson, S. P., Poole, R. K., Foster, S. J.
(1999). CtaA of Staphylococcus aureus Is Required for Starvation Survival, Recovery, and Cytochrome Biosynthesis. J. Bacteriol.
181: 501-507
[Abstract]
[Full Text]