Previous Article | Next Article 
Journal of Bacteriology, June 2005, p. 3650-3661, Vol. 187, No. 11
0021-9193/05/$08.00+0 doi:10.1128/JB.187.11.3650-3661.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
Bordetella AlcS Transporter Functions in Alcaligin Siderophore Export and Is Central to Inducer Sensing in Positive Regulation of Alcaligin System Gene Expression
Timothy J. Brickman and
Sandra K. Armstrong*
Department of Microbiology, University of Minnesota Medical School, Minneapolis, Minnesota 55455-0312
Received 13 December 2004/
Accepted 15 February 2005
Bordetella pertussis and Bordetella bronchiseptica, which are respiratory mucosal pathogens of mammals, produce and utilize the siderophore alcaligin to acquire iron in response to iron starvation. A predicted permease of the major facilitator superfamily class of membrane efflux pumps, AlcS (synonyms, OrfX and Bcr), was reported to be encoded within the alcaligin gene cluster. In this study, alcS null mutants were found to be defective in growth under iron starvation conditions, in iron source utilization, and in alcaligin export. trans complementation using cloned alcS genes of B. pertussis or B. bronchiseptica restored the wild-type phenotype to the alcS mutants. Although the levels of extracellular alcaligin measured in alcS strain culture fluids were severely reduced compared with the wild-type levels, alcS mutants had elevated levels of cell-associated alcaligin, implicating AlcS in alcaligin export. Interestingly, a
alcA mutation that eliminated alcaligin production suppressed the growth defects of alcS mutants. This suppression and the alcaligin production defect were reversed by trans complementation of the
alcA mutation in the double-mutant strain, confirming that the growth-defective phenotype of alcS mutants is associated with alcaligin production. In an alcA::mini-Tn5 lacZ1 operon fusion strain background, an alcS null mutation resulted in enhanced AlcR-dependent transcriptional responsiveness to alcaligin inducer; conversely, AlcS overproduction blunted the transcriptional response to alcaligin. These transcription studies indicate that the alcaligin exporter activity of AlcS is required to maintain appropriate intracellular alcaligin levels for normal inducer sensing and responsiveness necessary for positive regulation of alcaligin system gene expression.
* Corresponding author. Mailing address: Department of Microbiology, University of Minnesota, MMC 196, 420 Delaware Street S.E., Minneapolis, MN 55455-0312. Phone: (612) 625-6947. Fax: (612) 626-0623. E-mail:
sandra{at}mail.ahc.umn.edu.
Journal of Bacteriology, June 2005, p. 3650-3661, Vol. 187, No. 11
0021-9193/05/$08.00+0 doi:10.1128/JB.187.11.3650-3661.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Allard, K. A., Dao, J., Sanjeevaiah, P., McCoy-Simandle, K., Chatfield, C. H., Crumrine, D. S., Castignetti, D., Cianciotto, N. P.
(2009). Purification of Legiobactin and Importance of This Siderophore in Lung Infection by Legionella pneumophila. Infect. Immun.
77: 2887-2895
[Abstract]
[Full Text]
-
Miethke, M., Schmidt, S., Marahiel, M. A.
(2008). The Major Facilitator Superfamily-Type Transporter YmfE and the Multidrug-Efflux Activator Mta Mediate Bacillibactin Secretion in Bacillus subtilis. J. Bacteriol.
190: 5143-5152
[Abstract]
[Full Text]
-
Anderson, M. T., Armstrong, S. K.
(2008). Norepinephrine Mediates Acquisition of Transferrin-Iron in Bordetella bronchiseptica. J. Bacteriol.
190: 3940-3947
[Abstract]
[Full Text]
-
Brickman, T. J., Armstrong, S. K.
(2007). Impact of Alcaligin Siderophore Utilization on In Vivo Growth of Bordetella pertussis. Infect. Immun.
75: 5305-5312
[Abstract]
[Full Text]
-
Miethke, M., Marahiel, M. A.
(2007). Siderophore-Based Iron Acquisition and Pathogen Control. Microbiol. Mol. Biol. Rev.
71: 413-451
[Abstract]
[Full Text]
-
Quatrini, R., Lefimil, C., Veloso, F. A., Pedroso, I., Holmes, D. S., Jedlicki, E.
(2007). Bioinformatic prediction and experimental verification of Fur-regulated genes in the extreme acidophile Acidithiobacillus ferrooxidans. Nucleic Acids Res
35: 2153-2166
[Abstract]
[Full Text]
-
Diavatopoulos, D. A., Cummings, C. A., van der Heide, H. G. J., van Gent, M., Liew, S., Relman, D. A., Mooi, F. R.
(2006). Characterization of a Highly Conserved Island in the Otherwise Divergent Bordetella holmesii and Bordetella pertussis Genomes. J. Bacteriol.
188: 8385-8394
[Abstract]
[Full Text]
-
Anderson, M. T., Armstrong, S. K.
(2006). The Bordetella bfe system: growth and transcriptional response to siderophores, catechols, and neuroendocrine catecholamines.. J. Bacteriol.
188: 5731-5740
[Abstract]
[Full Text]
-
Allard, K. A., Viswanathan, V. K., Cianciotto, N. P.
(2006). lbtA and lbtB Are Required for Production of the Legionella pneumophila Siderophore Legiobactin. J. Bacteriol.
188: 1351-1363
[Abstract]
[Full Text]