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Infection and Immunity, April 2001, p. 2353-2363, Vol. 69, No. 4
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.4.2353-2363.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Involvement of HxuC Outer Membrane Protein in Utilization of Hemoglobin by Haemophilus influenzae

Leslie D. Cope,1 Robert P. Love,1 Sarah E. Guinn,1 Andrei Gilep,2 Sergei Usanov,2 Ronald W. Estabrook,2 Zbynek Hrkal,3 and Eric J. Hansen1,*

Departments of Microbiology1 and Biochemistry,2 University of Texas Southwestern Medical Center, Dallas, Texas 75390-9048, and Department of Cellular Biochemistry, Institute of Haemotology and Blood Transfusion, Prague, Czech Republic3

Received 18 May 2000/Returned for modification 12 July 2000/Accepted 16 January 2001

Haemophilus influenzae can utilize different protein-bound forms of heme for growth in vitro. A previous study from this laboratory indicated that nontypeable Haemophilus influenzae (NTHI) strain N182 expressed three outer membrane proteins, designated HgbA, HgbB, and HgbC, that bound hemoglobin or hemoglobin-haptoglobin and were encoded by open reading frames (ORFs) that contained a CCAA nucleotide repeat. Testing of mutants expressing the HgbA, HgbB, and HgbC proteins individually revealed that expression of any one of these proteins was sufficient to allow wild-type growth with hemoglobin. In contrast, mutants that expressed only HgbA or HgbC grew significantly better with hemoglobin-haptoglobin than did a mutant expressing only HgbB. Construction of an isogenic hgbA hgbB hgbC mutant revealed that the absence of these three gene products did not affect the ability of NTHI N182 to utilize hemoglobin as a source of heme, although this mutant was severely impaired in its ability to utilize hemoglobin-haptoglobin. The introduction of a tonB mutation into this triple mutant eliminated its ability to utilize hemoglobin, indicating that the pathway for hemoglobin utilization in the absence of HgbA, HgbB, and HgbC involved a TonB-dependent process. Inactivation in this triple mutant of the hxuC gene, which encodes a predicted TonB-dependent outer membrane protein previously shown to be involved in the utilization of free heme, resulted in loss of the ability to utilize hemoglobin. The results of this study reinforce the redundant nature of the heme acquisition systems expressed by H. influenzae.

* Corresponding author. Mailing address: Department of Microbiology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390-9048. Phone: (214) 648-5974. Fax: (214) 648-5905. E-mail: eric.hansen{at}UTSouthwestern.edu.

Infection and Immunity, April 2001, p. 2353-2363, Vol. 69, No. 4
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.4.2353-2363.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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