Stepwise transition of the tetra-manganese complex of Photosystem II to a binuclear Mn2(µ-O)2 complex in response to a temperature jump: an X-ray absorption spectroscopy study

Abstract

The manganese-complex of photosystem II (PSII) is the molecular basis of photosynthetic water oxidation. It contains 4 Mn atoms and, likely, 1 Ca ion. Electron densities on the D1-subunit of PSII obtained from protein crystallography were attributed to 4 Mn atoms lying about in one plane parallel to the membrane. This arrangement is incompatible with previous models of the Mn-complex. We used the controlled heating at 47°C of multilayers of PSII membrane fragments with the Mn-complex in the S1-redox state to obtain its stepwise dis-integration which was assayed by oxygen polarography, EPR- and X-ray absorption (XANES, EXAFS) spectroscopy. Two Mn-Mn distances of £ 2.702 and ~2.719 Å were detected in the control. A ~3.3 Å distance between heavy atoms (Mn/Ca) was lost after only 2 min of hea-ting, together with the oxygen evolution capability. Within 10 min of heating the loss of Mn-Mn distances of ~2.7 and ~3.1 Å occurred and 2 hexaquo Mn2+ ions were detected by EPR and EXAFS. The remaining 2 Mn atoms were still separated by ~2.7 Å. They were released as 2 Mn2+ within 3 h of heating. We tentatively interpret the effects of heating as follows: The Mn-complex in the S1-state consists of two di-µ-oxo bridged Mn-dimers; all Mn-Mn vectors are roughly parallel to the membrane plane. One dimer may bind one Ca ion; the Ca is rapidly released concomitantly with the inactivation of oxygen evolution. This process is followed by the reduction and release of the Ca-binding Mn-dimer (Mn-Mn distance £ 2.702 Å). The re-maining binuclear center is still a di-µ-oxo bridged MnIII2-dimer (Mn-Mn distance 2.719 Å).