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Journal of Bacteriology, October 1999, p. 6063-6072, Vol. 181, No. 19
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Use of Heme-Protein Complexes by the Yersinia enterocolitica HemR Receptor: Histidine Residues Are Essential for Receptor Function

Charles S. Bracken, Michael T. Baer, Asiya Abdur-Rashid, Whitney Helms, and Igor Stojiljkovic*

Department of Microbiology & Immunology, Emory University, Atlanta, Georgia 30322

Received 24 March 1999/Accepted 30 July 1999

The abilities of two bacterial active heme transporters, HmbR of Neisseria meningitidis and HemR of Yersinia enterocolitica, to use different heme sources were compared. While HmbR-expressing cells used only hemoglobin (Hb) and heme, HemR-expressing bacteria were able to grow on Hb, heme, myoglobin, hemopexin, catalase, human and bovine serum albumin-heme, and haptoglobin-hemoglobin complexes as sources of iron. Expression of functional HemR allowed Escherichia coli cells to respond to heme-containing peptides, microperoxidases MP-8, MP-9, and MP-11, suggesting the ability of HemR to transport heme covalently linked to other molecules. Comparison of HemR with other heme receptors identified several highly conserved histidine residues as well as two conserved amino acid motifs, the FRAP and NPNL boxes. A site-directed mutagenesis approach was used to investigate the roles of His128, His192, His352, and His461 residues in HemR function. The HemR receptor with histidine changed to lysine at position 128 (HemRH128K), HemRH461L, HemRH461A, and HemRH128A,H461A mutant receptors were unable to use Hb, human serum albumin-heme, and myoglobin as sources of porphyrin and iron. Utilization of free heme was also severely affected, with some residual heme uptake in cells expressing HemRH128K, HemRH461A, and HemRH461L. Conversely, the HemRH192T, HemRH352A, HemRH352K, and HemRH192T,H352K mutant receptors were fully functional. All mutant HemR proteins were expressed in the outer membrane at levels similar to that of the wild-type HemR receptor. Nonfunctional HemRs were able to bind heme- and Hb-agarose. A hypothetical model of the HemR function in which two conserved histidine residues, His128 and His461, participate in the transport of heme through the receptor pore is postulated.

* Corresponding author. Mailing address: Department of Microbiology & Immunology, Emory University, 1510 Clifton Rd., Atlanta, GA 30322. Phone: (404) 727-1322 or 727-5968. Fax: (404) 727-8250. E-mail: stojiljk{at}microbio1.microbio.emory.edu.

Journal of Bacteriology, October 1999, p. 6063-6072, Vol. 181, No. 19
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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