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Journal of Bacteriology, February 2003, p. 909-917, Vol. 185, No. 3
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.3.909-917.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Heme-Responsive Transcriptional Activation of Bordetella bhu Genes

Carin K. Vanderpool and Sandra K. Armstrong*

Department of Microbiology, University of Minnesota Medical School, Minneapolis, Minnesota 55455-0312

Received 26 August 2002/ Accepted 11 November 2002

Bordetella pertussis and Bordetella bronchiseptica, gram-negative respiratory pathogens of mammals, possess a heme iron utilization system encoded by the bhuRSTUV genes. Preliminary evidence suggested that expression of the BhuR heme receptor was stimulated by the presence of heme under iron-limiting conditions. The hurIR (heme uptake regulator) genes were previously identified upstream of the bhuRSTUV gene cluster and are predicted to encode homologs of members of the iron starvation subfamily of extracytoplasmic function (ECF) regulators. In this study, B. pertussis and B. bronchiseptica {Delta}hurI mutants, predicted to lack an ECF {sigma} factor, were constructed and found to be deficient in the utilization of hemin and hemoglobin. Genetic complementation of {Delta}hurI strains with plasmid-borne hurI restored wild-type levels of heme utilization. B. bronchiseptica {Delta}hurI mutant BRM23 was defective in heme-responsive production of the BhuR heme receptor; hurI in trans restored heme-inducible BhuR expression to the mutant and resulted in BhuR overproduction. Transcriptional analyses with bhuR-lacZ fusion plasmids confirmed that bhuR transcription was activated in iron-starved cells in response to heme compounds. Heme-responsive bhuR transcription was not observed in mutant BRM23, indicating that hurI is required for positive regulation of bhu gene expression. Furthermore, bhuR was required for heme-inducible bhu gene activation, supporting the hypothesis that positive regulation of bhuRSTUV occurs by a surface signaling mechanism involving the heme-iron receptor BhuR.

* Corresponding author. Mailing address: Department of Microbiology, University of Minnesota, MMC 196 FUMC, 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, February 2003, p. 909-917, Vol. 185, No. 3
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.3.909-917.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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