Reduction of the Mn cluster of the water-oxidizing enzyme by nitric oxide: formation of an S(-2) state

Biochemistry. 2002 Mar 5;41(9):3057-64. doi: 10.1021/bi015903z.

Abstract

The manganese cluster of the oxygen-evolving enzyme of photosystem II is chemically reduced upon interaction with nitric oxide at -30 degrees C. The state formed gives rise to an S = 1/2 multiline EPR signal [Goussias, Ch., Ioannidis, N., and Petrouleas, V. (1997) Biochemistry 36, 9261] that is attributed to a Mn(II)- Mn(III) dimer [Sarrou, J., Ioannidis, N., Deligiannakis, Y., and Petrouleas, V. (1998) Biochemistry 37, 3581]. In this work, we sought to establish whether the state could be assigned to a specific, reduced S state by using flash oxymetry, chlorophyll a fluorescence, and electron paramagnetic resonance spectroscopy. With the Joliot-type O(2) electrode, the first maximum of oxygen evolution was observed on the sixth or seventh flash. Three saturating pre-flashes were required to convert the flash pattern characteristic of NO-reduced samples to that of the untreated control (i.e., O(2) evolution maximum on the third flash). Measurements of the S state-dependent level of chlorophyll fluorescence in NO-treated PSII showed a three-flash downshift compared to untreated controls. In the EPR study, the maximum S(2) multi-line EPR signal was observed after the fourth flash. The results from all three methods are consistent with the Mn cluster being in a redox state corresponding to an S(-2) state in a majority of centers after treatment with NO. We were unable to generate the Mn(II)-Mn(III) multi-line signal using hydrazine as a reductant; it appears that the valence distribution and possibly the structure of the Mn cluster in the S(-2) state are dependent on the nature of the reductant that is used.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Electron Spin Resonance Spectroscopy
  • Enzymes / chemistry
  • Enzymes / metabolism
  • Fluorescence
  • Light-Harvesting Protein Complexes
  • Manganese / chemistry*
  • Nitric Oxide / chemistry*
  • Oxidation-Reduction
  • Photosynthetic Reaction Center Complex Proteins / chemistry*
  • Photosynthetic Reaction Center Complex Proteins / metabolism
  • Photosystem II Protein Complex
  • Time Factors
  • Water / chemistry*

Substances

  • Enzymes
  • Light-Harvesting Protein Complexes
  • Photosynthetic Reaction Center Complex Proteins
  • Photosystem II Protein Complex
  • Water
  • Nitric Oxide
  • Manganese