This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Saile, E.
Right arrow Articles by Koehler, T. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Saile, E.
Right arrow Articles by Koehler, T. M.

 Previous Article  |  Next Article 

Journal of Bacteriology, January 2002, p. 370-380, Vol. 184, No. 2
0021-9193/01/$04.00+0     DOI: 10.1128/JB.184.2.370-380.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Control of Anthrax Toxin Gene Expression by the Transition State Regulator abrB

Elke Saile and Theresa M. Koehler*

Department of Microbiology and Molecular Genetics, The University of Texas-Houston Health Science Center Medical School, Houston, Texas 77030

Received 17 August 2001/ Accepted 16 October 2001

Bacillus anthracis produces the anthrax toxin proteins protective antigen (PA), lethal factor (LF), and edema factor (EF) in a growth phase-dependent manner when cultured in liquid medium. Expression of the toxin genes pagA, lef, and cya peaks in late log phase, and steady-state levels of the toxin proteins are highest during the transition into stationary phase. Here we show that an apparent transition state regulator negatively regulates toxin gene expression. We identified two orthologues of the B. subtilis transition state regulator abrB in the B. anthracis genome: one on the chromosome and one on the 182-kb virulence plasmid pXO1. The orthologue located on the chromosome is predicted to encode a 94-amino-acid protein that is 85% identical to B. subtilis AbrB. The hypothetical protein encoded on pXO1 is 41% identical to B. subtilis AbrB but missing 27 amino acid residues from the amino terminus compared to the B. subtilis protein. Deletion of the pXO1-encoded abrB orthologue did not affect toxin gene expression under the conditions tested. However, a B. anthracis mutant in which the chromosomal abrB gene was deleted expressed pagA earlier and at a higher level than the parent strain. Expression of a transcriptional pagA-lacZ fusion in the abrB mutant was increased up to 20-fold during early exponential growth compared to the parent strain and peaked in mid-exponential rather than late exponential phase. In contrast to the strong effect of abrB on pagA expression, lef-lacZ and cya-lacZ expression during early-log-phase growth was increased only two- to threefold in the abrB null mutant. Western hybridization analysis showed increased PA, LF, and EF synthesis by the mutant. As is true in B. subtilis, the B. anthracis abrB gene is negatively regulated by spo0A. Our findings tie anthrax toxin gene expression to the complex network of postexponential phase adaptive responses that have been well studied in B. subtilis.

* Corresponding author. Mailing address: Department of Microbiology and Molecular Genetics, University of Texas-Houston Health Science Center Medical School, 6431 Fannin St., JFB 1.765, Houston, TX 77030. Phone: (713) 500-5450. Fax: (713) 500-5499. E-mail: Theresa.M.Koehler{at}uth.tmc.edu.

Journal of Bacteriology, January 2002, p. 370-380, Vol. 184, No. 2
0021-9193/01/$04.00+0     DOI: 10.1128/JB.184.2.370-380.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Underwood, S., Guan, S., Vijayasubhash, V., Baines, S. D., Graham, L., Lewis, R. J., Wilcox, M. H., Stephenson, K. (2009). Characterization of the Sporulation Initiation Pathway of Clostridium difficile and Its Role in Toxin Production. J. Bacteriol. 191: 7296-7305 [Abstract] [Full Text]  
  • van Schaik, W., Chateau, A., Dillies, M.-A., Coppee, J.-Y., Sonenshein, A. L., Fouet, A. (2009). The Global Regulator CodY Regulates Toxin Gene Expression in Bacillus anthracis and Is Required for Full Virulence. Infect. Immun. 77: 4437-4445 [Abstract] [Full Text]  
  • Sastalla, I., Chim, K., Cheung, G. Y. C., Pomerantsev, A. P., Leppla, S. H. (2009). Codon-Optimized Fluorescent Proteins Designed for Expression in Low-GC Gram-Positive Bacteria. Appl. Environ. Microbiol. 75: 2099-2110 [Abstract] [Full Text]  
  • Lucking, G., Dommel, M. K., Scherer, S., Fouet, A., Ehling-Schulz, M. (2009). Cereulide synthesis in emetic Bacillus cereus is controlled by the transition state regulator AbrB, but not by the virulence regulator PlcR. Microbiology 155: 922-931 [Abstract] [Full Text]  
  • Scaramozzino, F., White, A., Perego, M., Hoch, J. A. (2009). A Unique GTP-Dependent Sporulation Sensor Histidine Kinase in Bacillus anthracis. J. Bacteriol. 191: 687-692 [Abstract] [Full Text]  
  • Biswas, E. E., Barnes, M. H., Moir, D. T., Biswas, S. B. (2009). An Essential DnaB Helicase of Bacillus anthracis: Identification, Characterization, and Mechanism of Action. J. Bacteriol. 191: 249-260 [Abstract] [Full Text]  
  • Makarewicz, O., Neubauer, S., Preusse, C., Borriss, R. (2008). Transition State Regulator AbrB Inhibits Transcription of Bacillus amyloliquefaciens FZB45 Phytase through Binding at Two Distinct Sites Located within the Extended phyC Promoter Region. J. Bacteriol. 190: 6467-6474 [Abstract] [Full Text]  
  • Bongiorni, C., Fukushima, T., Wilson, A. C., Chiang, C., Mansilla, M. C., Hoch, J. A., Perego, M. (2008). Dual Promoters Control Expression of the Bacillus anthracis Virulence Factor AtxA. J. Bacteriol. 190: 6483-6492 [Abstract] [Full Text]  
  • Hadjifrangiskou, M., Koehler, T. M. (2008). Intrinsic curvature associated with the coordinately regulated anthrax toxin gene promoters. Microbiology 154: 2501-2512 [Abstract] [Full Text]  
  • Dong, S., McPherson, S. A., Tan, L., Chesnokova, O. N., Turnbough, C. L. Jr., Pritchard, D. G. (2008). Anthrose Biosynthetic Operon of Bacillus anthracis. J. Bacteriol. 190: 2350-2359 [Abstract] [Full Text]  
  • van Schaik, W., Prigent, J., Fouet, A. (2007). The stringent response of Bacillus anthracis contributes to sporulation but not to virulence. Microbiology 153: 4234-4239 [Abstract] [Full Text]  
  • Thompson, B. M., Waller, L. N., Fox, K. F., Fox, A., Stewart, G. C. (2007). The BclB Glycoprotein of Bacillus anthracis Is Involved in Exosporium Integrity. J. Bacteriol. 189: 6704-6713 [Abstract] [Full Text]  
  • Tinsley, E., Khan, S. A. (2007). A Bacillus anthracis-Based In Vitro System Supports Replication of Plasmid pXO2 as Well as Rolling-Circle-Replicating Plasmids. Appl. Environ. Microbiol. 73: 5005-5010 [Abstract] [Full Text]  
  • Bongiorni, C., Stoessel, R., Perego, M. (2007). Negative Regulation of Bacillus anthracis Sporulation by the Spo0E Family of Phosphatases. J. Bacteriol. 189: 2637-2645 [Abstract] [Full Text]  
  • Zeibell, K., Aguila, S., Yan Shi, V., Chan, A., Yang, H., Miller, J. H. (2007). Mutagenesis and Repair in Bacillus anthracis: the Effect of Mutators. J. Bacteriol. 189: 2331-2338 [Abstract] [Full Text]  
  • Hadjifrangiskou, M., Chen, Y., Koehler, T. M. (2007). The Alternative Sigma Factor {sigma}H Is Required for Toxin Gene Expression by Bacillus anthracis. J. Bacteriol. 189: 1874-1883 [Abstract] [Full Text]  
  • Ross, C. L., Koehler, T. M. (2006). plcR papR-Independent Expression of Anthrolysin O by Bacillus anthracis. J. Bacteriol. 188: 7823-7829 [Abstract] [Full Text]  
  • Heninger, S., Drysdale, M., Lovchik, J., Hutt, J., Lipscomb, M. F., Koehler, T. M., Lyons, C. R. (2006). Toxin-Deficient Mutants of Bacillus anthracis Are Lethal in a Murine Model for Pulmonary Anthrax. Infect. Immun. 74: 6067-6074 [Abstract] [Full Text]  
  • White, A. K., Hoch, J. A., Grynberg, M., Godzik, A., Perego, M. (2006). Sensor Domains Encoded in Bacillus anthracis Virulence Plasmids Prevent Sporulation by Hijacking a Sporulation Sensor Histidine Kinase.. J. Bacteriol. 188: 6354-6360 [Abstract] [Full Text]  
  • Klee, S. R., Ozel, M., Appel, B., Boesch, C., Ellerbrok, H., Jacob, D., Holland, G., Leendertz, F. H., Pauli, G., Grunow, R., Nattermann, H. (2006). Characterization of Bacillus anthracis-Like Bacteria Isolated from Wild Great Apes from Cote d'Ivoire and Cameroon.. J. Bacteriol. 188: 5333-5344 [Abstract] [Full Text]  
  • Bobay, B. G., Mueller, G. A., Thompson, R. J., Murzin, A. G., Venters, R. A., Strauch, M. A., Cavanagh, J. (2006). NMR Structure of AbhN and Comparison with AbrBN: FIRST INSIGHTS INTO THE DNA BINDING PROMISCUITY AND SPECIFICITY OF AbrB-LIKE TRANSITION STATE REGULATOR PROTEINS. J. Biol. Chem. 281: 21399-21409 [Abstract] [Full Text]  
  • Saile, E., Koehler, T. M. (2006). Bacillus anthracis Multiplication, Persistence, and Genetic Exchange in the Rhizosphere of Grass Plants.. Appl. Environ. Microbiol. 72: 3168-3174 [Abstract] [Full Text]  
  • Chitlaru, T., Gat, O., Gozlan, Y., Ariel, N., Shafferman, A. (2006). Differential Proteomic Analysis of the Bacillus anthracis Secretome: Distinct Plasmid and Chromosome CO2-Dependent Cross Talk Mechanisms Modulate Extracellular Proteolytic Activities.. J. Bacteriol. 188: 3551-3571 [Abstract] [Full Text]  
  • Janes, B. K., Stibitz, S. (2006). Routine Markerless Gene Replacement in Bacillus anthracis. Infect. Immun. 74: 1949-1953 [Abstract] [Full Text]  
  • Bongiorni, C., Stoessel, R., Shoemaker, D., Perego, M. (2006). Rap Phosphatase of Virulence Plasmid pXO1 Inhibits Bacillus anthracis Sporulation. J. Bacteriol. 188: 487-498 [Abstract] [Full Text]  
  • Pomerantsev, A. P., Sitaraman, R., Galloway, C. R., Kivovich, V., Leppla, S. H. (2006). Genome Engineering in Bacillus anthracis Using Cre Recombinase. Infect. Immun. 74: 682-693 [Abstract] [Full Text]  
  • Brunsing, R. L., La Clair, C., Tang, S., Chiang, C., Hancock, L. E., Perego, M., Hoch, J. A. (2005). Characterization of Sporulation Histidine Kinases of Bacillus anthracis. J. Bacteriol. 187: 6972-6981 [Abstract] [Full Text]  
  • Yao, F., Strauch, M. A. (2005). Independent and Interchangeable Multimerization Domains of the AbrB, Abh, and SpoVT Global Regulatory Proteins. J. Bacteriol. 187: 6354-6362 [Abstract] [Full Text]  
  • Vahling, C. M., McIver, K. S. (2005). Identification of Residues Responsible for the Defective Virulence Gene Regulator Mga Produced by a Natural Mutant of Streptococcus pyogenes. J. Bacteriol. 187: 5955-5966 [Abstract] [Full Text]  
  • Strauch, M. A., Ballar, P., Rowshan, A. J., Zoller, K. L. (2005). The DNA-binding specificity of the Bacillus anthracis AbrB protein. Microbiology 151: 1751-1759 [Abstract] [Full Text]  
  • Scotcher, M. C., Rudolph, F. B., Bennett, G. N. (2005). Expression of abrB310 and sinR, and Effects of Decreased abrB310 Expression on the Transition from Acidogenesis to Solventogenesis, in Clostridium acetobutylicum ATCC 824. Appl. Environ. Microbiol. 71: 1987-1995 [Abstract] [Full Text]  
  • Chen, Y., Tenover, F. C., Koehler, T. M. (2004). {beta}-Lactamase Gene Expression in a Penicillin-Resistant Bacillus anthracis Strain. Antimicrob. Agents Chemother. 48: 4873-4877 [Abstract] [Full Text]  
  • Daubenspeck, J. M., Zeng, H., Chen, P., Dong, S., Steichen, C. T., Krishna, N. R., Pritchard, D. G., Turnbough, C. L. Jr. (2004). Novel Oligosaccharide Side Chains of the Collagen-like Region of BclA, the Major Glycoprotein of the Bacillus anthracis Exosporium. J. Biol. Chem. 279: 30945-30953 [Abstract] [Full Text]  
  • Tinsley, E., Naqvi, A., Bourgogne, A., Koehler, T. M., Khan, S. A. (2004). Isolation of a Minireplicon of the Virulence Plasmid pXO2 of Bacillus anthracis and Characterization of the Plasmid-Encoded RepS Replication Protein. J. Bacteriol. 186: 2717-2723 [Abstract] [Full Text]  
  • Rasko, D. A., Ravel, J., Okstad, O. A., Helgason, E., Cer, R. Z., Jiang, L., Shores, K. A., Fouts, D. E., Tourasse, N. J., Angiuoli, S. V., Kolonay, J., Nelson, W. C., Kolsto, A.-B., Fraser, C. M., Read, T. D. (2004). The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. Nucleic Acids Res 32: 977-988 [Abstract] [Full Text]  
  • Drysdale, M., Bourgogne, A., Hilsenbeck, S. G., Koehler, T. M. (2004). atxA Controls Bacillus anthracis Capsule Synthesis via acpA and a Newly Discovered Regulator, acpB. J. Bacteriol. 186: 307-315 [Abstract] [Full Text]  
  • Liu, H., Bergman, N. H., Thomason, B., Shallom, S., Hazen, A., Crossno, J., Rasko, D. A., Ravel, J., Read, T. D., Peterson, S. N., Yates, J. III, Hanna, P. C. (2004). Formation and Composition of the Bacillus anthracis Endospore. J. Bacteriol. 186: 164-178 [Abstract] [Full Text]  
  • Pomerantsev, A. P., Kalnin, K. V., Osorio, M., Leppla, S. H. (2003). Phosphatidylcholine-Specific Phospholipase C and Sphingomyelinase Activities in Bacteria of the Bacillus cereus Group. Infect. Immun. 71: 6591-6606 [Abstract] [Full Text]  
  • Ariel, N., Zvi, A., Makarova, K. S., Chitlaru, T., Elhanany, E., Velan, B., Cohen, S., Friedlander, A. M., Shafferman, A. (2003). Genome-Based Bioinformatic Selection of Chromosomal Bacillus anthracis Putative Vaccine Candidates Coupled with Proteomic Identification of Surface-Associated Antigens. Infect. Immun. 71: 4563-4579 [Abstract] [Full Text]  
  • Bourgogne, A., Drysdale, M., Hilsenbeck, S. G., Peterson, S. N., Koehler, T. M. (2003). Global Effects of Virulence Gene Regulators in a Bacillus anthracis Strain with Both Virulence Plasmids. Infect. Immun. 71: 2736-2743 [Abstract] [Full Text]  
  • Ariel, N., Zvi, A., Grosfeld, H., Gat, O., Inbar, Y., Velan, B., Cohen, S., Shafferman, A. (2002). Search for Potential Vaccine Candidate Open Reading Frames in the Bacillus anthracis Virulence Plasmid pXO1: In Silico and In Vitro Screening. Infect. Immun. 70: 6817-6827 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»