Functional roles of the [2Fe-2S] clusters in Synechocystis PCC 6803 Hox [NiFe]-hydrogenase reactivity with ferredoxins

J Biol Chem. 2024 Dec;300(12):107936. doi: 10.1016/j.jbc.2024.107936. Epub 2024 Oct 28.

Abstract

The HoxEFUYH complex of Synechocystis PCC 6803 (S. 6803) consists of a HoxEFU ferredoxin:NAD(P)H oxidoreductase subcomplex and a HoxYH [NiFe]-hydrogenase subcomplex that catalyzes reversible H2 oxidation. Prior studies have suggested that the presence of HoxE is required for reactivity with ferredoxin; however, it is unknown how HoxE is functionally integrated into the electron transfer network of the HoxEFU:ferredoxin complex. Deciphering electron transfer pathways is challenged by the rich iron-sulfur cluster content of HoxEFU, which includes a [2Fe-2S] cluster in each subunit, along with multiple [4Fe-4S] clusters and a flavin cofactor. To resolve the role of HoxE, we determined the biophysical and thermodynamic properties of each [2Fe-2S] cluster in HoxEFU using steady-state and potentiometric EPR analysis in combination with square wave voltammetry (SWV). The temperature-dependence of the EPR signal for HoxE confirmed the coordination of a single [2Fe-2S] cluster that was shown by SWV to have an Em = -424 mV (versus SHE). Strikingly, when the Em of the HoxE [2Fe-2S] cluster was analyzed in HoxEFU titrations, it was shifted by >100 mV to an Em < -525 mV (versus SHE). EPR titrations of HoxEFU gave an Em value for the [2Fe-2S] cluster of HoxF, Em = -419 mV and HoxU, Em = -349 mV. These values were used to re-analyze the diaphorase kinetics in reactions performed with ferredoxins with varying Em's. The results are formulated into a model of HoxEFU:ferredoxin reactivity and the role of HoxE in mediating electron transfer within the HoxEFU:ferredoxin complex.

Keywords: EPR; Synechocystis; [NiFe]-hydrogenase; diaphorase; electron transfer; ferredoxin; iron-sulfur cluster; redox potential; square wave voltammetry.

MeSH terms

  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Electron Spin Resonance Spectroscopy
  • Electron Transport
  • Ferredoxins* / chemistry
  • Ferredoxins* / metabolism
  • Hydrogenase* / chemistry
  • Hydrogenase* / genetics
  • Hydrogenase* / metabolism
  • Iron-Sulfur Proteins / chemistry
  • Iron-Sulfur Proteins / metabolism
  • Oxidation-Reduction
  • Synechocystis* / enzymology
  • Synechocystis* / metabolism
  • Thermodynamics

Substances

  • Hydrogenase
  • nickel-iron hydrogenase
  • Ferredoxins
  • Bacterial Proteins
  • Iron-Sulfur Proteins