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Binding of Pseudomonas aeruginosa Apobacterioferritin-Associated Ferredoxin to Bacterioferritin B Promotes Heme Mediation of Electron Delivery and Mobilization of Core Mineral Iron

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Ralph N. Adams Institute for Bioanalytical Chemistry and Department of Chemistry, University of Kansas, Multidisciplinary Research Building, 2030 Becker Drive, Room 220 E, Lawrence, Kansas 66047
§ Structural Biology Center, University of Kansas, 2121 Simons Drive, Lawrence, Kansas 66047
*To whom correspondence should be addressed. Phone: 785-864-4936. Fax: 785-864-5396. E-mail: [email protected]
∥Current address: Department of Pharmaceutical Chemistry, University of Kansas, Lawrence, KS 66047
Cite this: Biochemistry 2009, 48, 31, 7420–7431
Publication Date (Web):July 4, 2009
https://doi.org/10.1021/bi900561a
Copyright © 2009 American Chemical Society

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    The bfrB gene from Pseudomonas aeruginosa was cloned and expressed in Escherichia coli. The resultant protein (BfrB), which assembles into a 445.3 kDa complex from 24 identical subunits, binds 12 molecules of heme axially coordinated by two Met residues. BfrB, isolated with 5−10 iron atoms per protein molecule, was reconstituted with ferrous ions to prepare samples with a core mineral containing 600 ± 40 ferric ions per BfrB molecule and approximately one phosphate molecule per iron atom. In the presence of sodium dithionite or in the presence of P. aeruginosa ferredoxin NADP reductase (FPR) and NADPH, the heme in BfrB remains oxidized, and the core iron mineral is mobilized sluggishly. In stark contrast, addition of NADPH to a solution containing BfrB, FPR, and the apo form of P. aeruginosa bacterioferritin-associated ferredoxin (apo-Bfd) results in rapid reduction of the heme in BfrB and in the efficient mobilization of the core iron mineral. Results from additional experimentation indicate that Bfd must bind to BfrB to promote heme mediation of electrons from the surface to the core to support the efficient mobilization of ferrous ions from BfrB. In this context, the thus far mysterious role of heme in bacterioferritins has been brought to the front by reconstituting BfrB with its physiological partner, apo-Bfd. These findings are discussed in the context of a model for the utilization of stored iron in which the significant upregulation of the bfd gene under low-iron conditions [Ochsner, U. A., Wilderman, P. J., Vasil, A. I., and Vasil, M. L. (2002) Mol. Microbiol. 45, 1277−1287] ensures sufficient concentrations of apo-Bfd to bind BfrB and unlock the iron stored in its core. Although these findings are in contrast to previous speculations suggesting redox mediation of electron transfer by holo-Bfd, the ability of apo-Bfd to promote iron mobilization is an economical strategy used by the cell because it obviates the need to further deplete cellular iron levels to assemble iron−sulfur clusters in Bfd before the iron stored in BfrB can be mobilized and utilized.

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    DNA sequence of BfrB from P. aeruginosa engineered with silent mutations to include codons favored by E. coli and electronic absorption spectra of oxidized wild-type and C43S Bfd. This material is available free of charge via the Internet at http://pubs.acs.org.

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