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Transcriptional Control of the rhuIR-bhuRSTUV Heme Acquisition Locus in Bordetella avium

Witebsky Center for Microbial Pathogenesis and Immunology,¹ Department of Microbiology and Immunology,² Department of Oral Biology, University at Buffalo, State University of New York, Buffalo, New York³

Received 16 August 2004/ Returned for modification 20 September 2004/ Accepted 6 November 2004

Iron (Fe) is an essential nutrient for most bacterial pathogens. In these organisms, a variety of regulatory systems that respond to specific Fe complexes found within their vertebrate hosts have evolved. In Bordetella avium, the heme utilization locus encoded by rhuIR-bhuRSTUV mediates efficient acquisition of Fe from heme and hemoproteins. Control of bhuRSTUV expression is promulgated at two levels. When Fe is abundant, expression is repressed in a Fur-dependent manner which is partially relieved when Fe is limiting. In the presence of heme or hemoproteins, expression of the bhuRSTUV operon is induced via a three-component signal transduction cascade composed of RhuI, RhuR, and BhuR. Herein, we report the identification of two promoters (P_rhuI and P_bhuR) that control expression of the rhuIR-bhuRSTUV cluster. Primer extension analysis identified the transcriptional start site of P_rhuI within a putative Fur box. Transcriptional initiation of P_bhuR mapped within the rhuR-bhuR intergenic region. Maximal transcription from P_bhuR required Fe-limiting conditions, the presence of heme (or hemoglobin), and rhuI; however, analysis of transcripts produced from the rhuIR-bhuRSTUV locus revealed a pattern of low-level bhuR transcription in the absence of heme which originated from both P_bhuR and P_rhuI. Transcription from P_rhuI was repressed by Fe in the presence of fur and somewhat enhanced by the addition of hemin to Fe-limited media. The nature of this hemin-associated P_rhuI stimulation was rhuI independent and therefore not induced by heme via the BhuR-RhuR-RhuI signal cascade. Fe also repressed transcription from P_bhuR in a fur-dependent manner; however, activation from this promoter, in the presence or absence of heme, did not occur without rhuI.

Editor: J. T. Barbieri

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