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Intermolecular electron transfer in two-iron superoxide reductase: a putative role for the desulforedoxin center as an electron donor to the iron active site

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Abstract

Superoxide reductase (SOR) is a superoxide detoxification system present in some microorganisms. Its active site consists of an unusual mononuclear iron center with an FeN4S1 coordination which catalyzes the one-electron reduction of superoxide to form hydrogen peroxide. Different classes of SORs have been described depending on the presence of an additional rubredoxin-like, desulforedoxin iron center, whose function has remained unknown until now. In this work, we investigated the mechanism of the reduction of the SOR iron active site using the NADPH:flavodoxin oxidoreductase from Escherichia coli, which was previously shown to efficiently transfer electrons to the Desulfoarculus baarsii SOR. When present, the additional rubredoxin-like iron center could function as an electronic relay between cellular reductases and the iron active site for superoxide reduction. This electron transfer was mainly intermolecular, between the rubredoxin-like iron center of one SOR and the iron active site of another SOR. These data provide the first experimental evidence for a possible role of the rubredoxin-like iron center in the superoxide detoxifying activity of SOR.

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Notes

  1. The semireduced form of SOR corresponds to the air-isolated protein, where center I is ferric and center II is ferrous.

Abbreviations

Fpr:

NADPH:flavodoxin oxidoreductase

ROS:

Reduced oxygen species

SOR:

Superoxide reductase

Tris:

Tris(hydoxymethyl)aminomethane

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Acknowledgments

We thank Jean-Marc Moulis for providing us with rubredoxin from Clostridium pasteurianum and Vincent Favaudon for kind assistance in pulse radiolysis experiments. V.N. and S.D. acknowledge support from the Agence Nationale de la Recherche, programme Physique et Chimie du Vivant 2008. We thank the language center of René Descartes University and Sam Shen for proofreading the manuscript.

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Author notes

  1. Julien Valton

    Present address: Cellectis Bioresearch, 102 Avenue Gaston Roussel, 93230, Romainville, France

Authors and Affiliations

  1. Laboratoire de Chimie et Biologie des Métaux, iRTSV-CEA Grenoble/CNRS/Université Joseph Fourier, 17 Avenue des Martyrs, 38054, Grenoble Cedex 9, France

    Florence Bonnot, Simon Duval, Julien Valton & Vincent Nivière

  2. Laboratoire de Chimie et Biochimie Pharmacologiques et Toxicologiques, UMR 8601, Université René Descartes Paris 5, 45 Rue des Saints-Pères, 75270, Paris Cedex 06, France

    Murielle Lombard

  3. Laboratoire de Chimie Physique, Centre Universitaire, UMR 8000 CNRS/Université Paris-Sud and CNRS, Bâtiment 350, 91405, Orsay Cedex, France

    Chantal Houée-Levin

Authors
  1. Florence Bonnot
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  2. Simon Duval
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  3. Murielle Lombard
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Correspondence to Vincent Nivière.

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Bonnot, F., Duval, S., Lombard, M. et al. Intermolecular electron transfer in two-iron superoxide reductase: a putative role for the desulforedoxin center as an electron donor to the iron active site. J Biol Inorg Chem 16, 889–898 (2011). https://doi.org/10.1007/s00775-011-0788-5

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