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J. Biol. Chem., Vol. 279, Issue 43, 44384-44393, October 22, 2004

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The Iron Superoxide Dismutase from the Filamentous Cyanobacterium Nostoc PCC 7120

LOCALIZATION, OVEREXPRESSION, AND BIOCHEMICAL CHARACTERIZATION^*

Günther Regelsberger, Ulrike Laaha, Dagmar Dietmann, Florian Rüker, Antonella Canini¶, Maria Grilli-Caiola¶, Paul Georg Furtmüller, Christa Jakopitsch, Günter A. Peschek||, and Christian Obinger**

From the Department of Chemistry, Division of Biochemistry, Metalloprotein Research Group, BOKU, University of Natural Resources and Applied Life Sciences, Muthgasse 18, A-1190 Vienna, Austria, the Department of Biotechnology, BOKU, University of Natural Resources and Applied Life Sciences, Muthgasse 18, A-1190 Vienna, Austria, the ^¶Department of Biology, University of Rome Tor Vergata, Via della Ricerca Scientifica 1, I-00133 Rome, Italy, and the ^||Institute of Physical Chemistry, Molecular Bioenergetics Group, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria

The nitrogen-fixing filamentous cyanobacterium Nostoc PCC 7120 (formerly named Anabaena PCC 7120) possesses two genes for superoxide dismutase, a unique membrane-associated manganese superoxide dismutase (MnSOD) and a soluble iron superoxide dismutase (FeSOD). A phylogenetic analysis of FeSODs shows that cyanobacterial enzymes form a well separated cluster with filamentous species found in one subcluster and unicellular species in the other. Activity staining, inhibition patterns, and immunogold labeling show that FeSOD is localized in the cytosol of vegetative cells and heterocysts (nitrogenase containing specialized cells formed during nitrogen-limiting conditions). The recombinant Nostoc FeSOD is a homodimeric, acidic enzyme exhibiting the characteristic iron peak at 350 nm in its ferric state, an almost 100% occupancy of iron per subunit, a specific activity using the ferricytochrome assay of (2040 ± 90) units mg^–1 at pH 7.8, and a dissociation constant K_d of the azide-FeSOD complex of 2.1 mM. Using stopped flow spectroscopy it was shown that the decay of superoxide in the presence of various FeSOD concentrations is first-order in enzyme concentration allowing the calculation of the catalytic rate constants, which increase with decreasing pH: 5.3 x 10⁹ M^–1 s^–1 (pH 7) to 4.8 x 10⁶ M^–1 s^–1 (pH 10). FeSOD and MnSOD complement each other to keep the superoxide level low in Nostoc PCC 7120, which is discussed with respect to the fact that Nostoc PCC 7120 exhibits oxygenic photosynthesis and oxygen-dependent respiration within a single prokaryotic cell and also has the ability to form differentiated cells under nitrogen-limiting conditions.

Received for publication, June 4, 2004 , and in revised form, July 28, 2004.

^* This work was supported by the Austrian Science Fund (FWF-Project P13069-CHE). 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. Fax: 43-1-36006-6059; E-mail: christian.obinger{at}boku.ac.at.

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