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Infection and Immunity, October 2002, p. 5390-5403, Vol. 70, No. 10
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.10.5390-5403.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

BhuR, a Virulence-Associated Outer Membrane Protein of Bordetella avium, Is Required for the Acquisition of Iron from Heme and Hemoproteins

Erin R. Murphy,1 Randy E. Sacco,2 Amy Dickenson,1 Daniel J. Metzger,1 Yan Hu,1 Paul E. Orndorff,3 and Terry D. Connell1*

The Witebsky Center for Microbial Pathogenesis and Immunology and Department of Microbiology, School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York 14214,1 Respiratory Disease Unit, National Animal Disease Center, Ames, Iowa 50010,2 Department of Microbiology, Pathology, and Parasitology, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina 276063

Received 17 April 2002/ Returned for modification 7 June 2002/ Accepted 27 June 2002

Iron (Fe) is an essential element for most organisms which must be obtained from the local environment. In the case of pathogenic bacteria, this fundamental element must be acquired from the fluids and tissues of the infected host. A variety of systems have evolved in bacteria for efficient acquisition of host-bound Fe. The gram-negative bacterium Bordetella avium, upon colonization of the avian upper respiratory tract, produces a disease in birds that has striking similarity to whooping cough, a disease caused by the obligate human pathogen Bordetella pertussis. We describe a B. avium Fe utilization locus comprised of bhuR and six accessory genes (rhuIR and bhuSTUV). Genetic manipulations of B. avium confirmed that bhuR, which encodes a putative outer membrane heme receptor, mediates efficient acquisition of Fe from hemin and hemoproteins (hemoglobin, myoglobin, and catalase). BhuR contains motifs which are common to bacterial heme receptors, including a consensus FRAP domain, an NPNL domain, and two TonB boxes. An N-terminal 32-amino-acid segment, putatively required for rhuIR-dependent regulated expression of bhuR, is present in BhuR but not in other bacterial heme receptors. Two forms of BhuR were observed in the outer membrane of B. avium: a 91-kDa polypeptide consistent in size with the predicted mature protein and a smaller 82-kDa polypeptide which lacks the 104 amino acids found at the N terminus of the 91-kDa form. A mutation in hemA was engineered in B. avium to demonstrate that the bacterium transports heme into the cytoplasm in a BhuR-dependent manner. The role of BhuR in virulence was established in turkey poults by use of a competitive-infection model.

* Corresponding author. Mailing address: The Witebsky Center for Microbial Pathogenesis and Immunology and Department of Microbiology, School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, NY 14214. Phone: (716) 829-3364. Fax: (716) 829-2158. E-mail: connell{at}acsu.buffalo.edu.

Editor: J. T. Barbieri

Infection and Immunity, October 2002, p. 5390-5403, Vol. 70, No. 10
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.10.5390-5403.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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