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J. Biol. Chem., Vol. 281, Issue 38, 27827-27835, September 22, 2006

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Paired Bacillus anthracis Dps (Mini-ferritin) Have Different Reactivities with Peroxide^*

Xiaofeng Liu, Kijeong Kim^¶, Terrance Leighton, and Elizabeth C. Theil¹

From the Children's Hospital Oakland Research Institute, Oakland, California 94609, Department of Nutritional Science and Toxicology, University of California, Berkeley, California 94720, and ^¶Department of Microbiology, Chung-Ang University College of Medicine, Seoul 156-756, Korea

Dps (DNA protection during starvation) proteins, mini-ferritins in the ferritin superfamily, catalyze Fe²⁺/H₂O₂/O₂ reactions and make minerals inside protein nanocages to minimize radical oxygen-chemistry (metal/osmotic/temperature/nutrient/oxidant) and sometimes to confer virulence. Paired Dps proteins in Bacillus, rare in other bacteria, have 60% sequence identity. To explore functional differences in paired Bacilli Dps protein, we measured ferroxidase activity and DNA protection (hydroxyl radical) for Dps protein dodecamers from Bacillus anthracis (Ba) since crystal structures and iron mineralization (iron-stain) were known. The self-assembled (200 kDa) Ba Dps1 (Dlp-1) and Ba Dps2 (Dlp-2) proteins had similar Fe²⁺/O₂ kinetics, with space for minerals of 500 iron atoms/protein, and protected DNA. The reactions with Fe²⁺ were novel in several ways: 1) Ba Dps2 reactions (Fe²⁺/H₂O₂) proceeded via an A_{650 nm} intermediate, with similar rates to maxi-ferritins (Fe²⁺/O₂), indicating a new Dps protein reaction pathway, 2) Ba Dps2 reactions (Fe²⁺/O₂ versus Fe²⁺/O₂ + H₂O₂) differed 3-fold contrasting with Escherichia coli Dps reactions, with 100-fold differences, and 3) Ba Dps1, inert in Fe²⁺/H₂O₂ catalysis, inhibited protein-independent Fe²⁺/H₂O₂ reactions. Sequence similarities between Ba Dps1 and Bacillus subtilis DpsA (Dps1), which is regulated by general stress factor (SigmaB) and Fur, and between Ba Dps2 and B. subtilis MrgA, which is regulated by H₂O₂ (PerR), suggest the function of Ba Dps1 is iron sequestration and the function of Ba Dps2 is H₂O₂ destruction, important in host/pathogen interactions. Destruction of H₂O₂ by Ba Dps2 proceeds via an unknown mechanism with an intermediate similar spectrally (A_{650 nm}) and kinetically to the maxi-ferritin diferric peroxo complex.

Received for publication, February 14, 2006 , and in revised form, June 26, 2006.

^* This work was supported by National Institutes of Health Grant DK-20251 (to X. L. and E. C. T.), Cooley's Anemia Foundation (to X. L.), and Defense Advanced Research Projects Agency (to K. K. and T. L.). 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.

¹ To whom correspondence should be addressed: Children's Hospital Oakland Research Institute, 5700 Martin Luther King, Jr. Way, Oakland, CA 94609. Tel.: 510-450-7670; Fax: 510-597-7131; E-mail: etheil{at}chori.org.

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