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J. Biol. Chem., Vol. 280, Issue 30, 28095-28102, July 29, 2005

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A Novel Porphyromonas gingivalis FeoB Plays a Role in Manganese Accumulation^*

Stuart G. Dashper, Catherine A. Butler, J. Patricia Lissel, Rita A. Paolini, Brigitte Hoffmann, Paul D. Veith, Neil M. O'Brien-Simpson, Sarah L. Snelgrove, John T. Tsiros, and Eric C. Reynolds¶

From the Center for Oral Health Science, School of Dental Science, The University of Melbourne, Victoria 3010, Australia and the School of Geosciences, Monash University, Wellington Road, Clayton, Victoria 3168, Australia

FeoB is an atypical transporter that has been shown to exclusively mediate ferrous ion transport in some bacteria. Unusually the genome of the periodontal pathogen Porphyromonas gingivalis has two genes (feoB1 and feoB2) encoding FeoB homologs, both of which are expressed in bicistronic operons. Kinetic analysis of ferrous ion transport by P. gingivalis W50 revealed the presence of a single, high affinity system with a K_t of 0.31 µM. FeoB1 was found to be solely responsible for this transport as energized cells of the isogenic FeoB1 mutant (W50FB1) did not transport radiolabeled iron, while the isogenic FeoB2 mutant (W50FB2) transported radiolabeled iron at a rate similar to wild type. This was reflected in the iron content of W50FB1 grown in iron excess conditions which was approximately half that of the wild type and W50FB2. The W50FB1 mutant had increased sensitivity to both oxygen and hydrogen peroxide and was avirulent in an animal model of infection whereas W50FB2 exhibited the same virulence as the wild type. Analysis of manganous ion uptake using inductively coupled plasma-mass spectrometry revealed a greater than 3-fold decrease in intracellular manganese accumulation in W50FB2 which was also unable to grow in manganese-limited media. The protein co-expressed with FeoB2 appears to be a novel FeoA-MntR fusion protein that exhibits homology to a manganese-responsive, DNA-binding metalloregulatory protein. These results indicate that FeoB2 is not involved in iron transport but plays a novel role in manganese transport.

Received for publication, April 11, 2005 , and in revised form, May 13, 2005.

^* This work was supported by an Australian National Health and Medical Research Council project grant. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ To whom correspondence should be addressed. Tel.: 61-3-9341-0270; Fax: 61-3-9341-0236; E-mail: e.reynolds{at}unimelb.edu.au.

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