Structural characterization of NAD(P)H:quinone oxidoreductase WrbA from E. coli in complex with benzoquinone

O. Degtjarik1, J. Brynda2, D. Reha1,3, J. Carrey4, I. Kuta Smatanova1,3 and R. Ettrich1,3

1University of South Bohemia, Faculty of Science, Branišovska 31, CZ-37005 Česke Budejovice, Czech Republic

2Institute of Molecular Genetics of the Academy of Science of the Czech Republic, v.v.i., Flemingovo no. 2, 16637 Prague, Czech Republic

3Academy of Sciences of the Czech Republic, Institute of Nanobiology and Structural Biology GCRC, Zamek 136, 373 33 Nove Hrady, Czech Republic

4Department of Chemistry, Princeton University, Princeton, NJ 08544-1009, USA

 

The protein WrbA from E. coli belongs to the family of flavodoxine-like proteins and participates in protection of bacterial cell from oxidative stress. It acts as a homotertamer with one molecule of FMN specifically bound per protein monomer as a co-factor. WrbA catalyses transfer of two electrons from NADH to electron acceptor using a ping-pong kinetic mechanism, where oxidized quinone binds after NAD moves out from the active site. Similar kinetic mechanism, presence of analogous co-factor and common structural features demonstrate the close relationship of WrbA with eukaryotic dimeric FAD-dependent oxidoreductases.

In order to understand the structural basics of benzoquinone binding and probable mechanism of quinone reduction we have determined the crystal structure of WrbA in complex with FMN and benzoquinone at 1.33 Å resolution. WrbA adopts α/β-twisted open-sheet fold typical for flavodoxines. Three monomers contribute to each of four identical active sites. The molecule of benzoquinone is stacked in the active site between aromatic ring of FMN and Trp97, which is the ideal position for electron transfer tested by QM/MM calculations of charge transfer rates. Comparison of the structure of WrbA-FMN benzoquinone complex with the structure of dimeric mammalian oxidoreductase in complex with duroquinone (pdb id 1qrd) reveals similar monomeric fold and the position of the quinone ring. The active site of WrbA is fully occupied by benzoquinone and cannot accommodate the second substrate NADH. This finding is consistent with ping-pong kinetic mechanism proposed for WrbA.

This work was supported by the Czech Science Foundation (project no P207/10/1934).