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Molecular Pathogenesis

Transcriptional Regulation of the Heme Binding Protein Gene Family of Bartonella quintana Is Accomplished by a Novel Promoter Element and Iron Response Regulator

James M. Battisti, Laura S. Smitherman, Kate N. Sappington, Nermi L. Parrow, Rahul Raghavan, Michael F. Minnick
James M. Battisti
Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
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Laura S. Smitherman
Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
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Kate N. Sappington
Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
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Nermi L. Parrow
Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
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Rahul Raghavan
Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
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Michael F. Minnick
Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
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  • For correspondence: mike.minnick@mso.umt.edu
DOI: 10.1128/IAI.00497-07
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ABSTRACT

We previously identified a five-member family of hemin-binding proteins (Hbp's) of Bartonella quintana that bind hemin on the outer surface but share no homology with known bacterial heme receptors. Subsequently, we demonstrated that expression of the hbp family is significantly influenced by oxygen, heme, and temperature conditions encountered by the pathogen in the human host and the body louse vector; e.g., we observed a dramatic (>100-fold) increase in hbpC transcript levels in response to the “louse-like” temperature of 30°C. The goal of the present study was to identify a transcription factor(s) involved in the coordinated and differential regulation of the hbp family. First, we used quantitative real-time PCR (qRT-PCR) to show that the same environmental conditions generate parallels in the transcript profiles of four candidate transcriptional regulators (Irr, Fur, RirA, and BatR) described in the order Rhizobiales, with the greatest overall change in the transcription of irr (a >5-fold decrease) at a “louse-like” temperature, suggesting that Irr may function as an hbpC repressor. Second, a B. quintana strain hyperexpressing Irr was constructed; it exhibits a “bloodstream-like” hbp transcript profile in the absence of an environmental stimulus (i.e., hbpC is repressed and hbpA, hbpD, and hbpE mRNAs are relatively abundant). Furthermore, when this strain is grown at a “louse-like” temperature, an inversion of the transcript profile occurs, where derepression of hbpC and repression of hbpA, hbpD, and hbpE are readily evident, strongly suggesting that Irr and temperature influence hbp family expression. Third, electrophoretic mobility shift analyses show that recombinant Irr binds specifically to the hbpC promoter region at a sequence that is highly conserved in Bartonella hbp genes, which we designated the hbp family box, or “H-box.” Fourth, we used the H-box to search the B. quintana genome and discovered a number of intriguing open reading frames, e.g., five members of a six-member family of cohemolysin autotransporters. Finally, qRT-PCR data regarding the effects of Fur and RirA overexpression on the hbp family are provided; they show that Fur's effect on the hbp family is relatively minor but RirA generates a “bloodstream-like” hbp transcript profile in the absence of an environmental stimulus, as observed for the Irr-hyperexpressing strain.

  • Copyright © 2007 American Society for Microbiology
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Transcriptional Regulation of the Heme Binding Protein Gene Family of Bartonella quintana Is Accomplished by a Novel Promoter Element and Iron Response Regulator
James M. Battisti, Laura S. Smitherman, Kate N. Sappington, Nermi L. Parrow, Rahul Raghavan, Michael F. Minnick
Infection and Immunity Aug 2007, 75 (9) 4373-4385; DOI: 10.1128/IAI.00497-07

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Transcriptional Regulation of the Heme Binding Protein Gene Family of Bartonella quintana Is Accomplished by a Novel Promoter Element and Iron Response Regulator
James M. Battisti, Laura S. Smitherman, Kate N. Sappington, Nermi L. Parrow, Rahul Raghavan, Michael F. Minnick
Infection and Immunity Aug 2007, 75 (9) 4373-4385; DOI: 10.1128/IAI.00497-07
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KEYWORDS

Bacterial Proteins
Bartonella quintana
Carrier Proteins
Gene Expression Regulation, Bacterial
Hemeproteins
Multigene Family
Pediculus
Promoter Regions, Genetic
transcription factors
Transcription, Genetic

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