X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution

Abstract

The mechanism by which the Mn-containing oxygen evolving complex (OEC) produces oxygen from water has been of great interest for over 40 years. This review focuses on how X-ray spectroscopy has provided important information about the structure of this Mn complex and its intermediates, or S-states, in the water oxidation cycle. X-ray absorption near-edge structure spectroscopy and high-resolution Mn Kbeta X-ray emission spectroscopy experiments have identified the oxidation states of the Mn in the OEC in each of the intermediate S-states, while extended X-ray absorption fine structure experiments have shown that 2.7 A Mn-Mn di-mu-oxo and 3.3 A Mn-Mn mono-mu-oxo motifs are present in the OEC. X-ray spectroscopy has also been used to probe the two essential cofactors in the OEC, Ca2+ and Cl-, and has shown that Ca2+ is an integral component of the OEC and is proximal to Mn. In addition, dichroism studies on oriented PS II membranes have provided angular information about the Mn-Mn and Mn-Ca vectors. Based on these X-ray spectroscopy data, refined models for the structure of the OEC and a mechanism for oxygen evolution by the OEC are presented.

Biosynthetic Ca2+/Sr2+ Exchange in the Photosystem II Oxygen-evolving Enzyme of Thermosynechococcus elongatus

“…50), it seems reasonable that the main influence of Sr 2ϩ will be on its nearest neighbors, the Tyr Z and particularly the Mn 4 . A slowdown in the forward steps of the enzyme cycle (the advancement of the S-states) and the associated lowering of oxygen-evolving activity, as reported here and earlier, fit with the existing ideas on the location and role of the Ca 2ϩ .…”

“…Absorption of a photon results in a charge separation between a chlorophyll molecule (P 680 ), and a pheophytin molecule. The pheophytin anion transfers the electron to a quinone, Q A , and P 680 ϩ is reduced by a tyrosine residue, Tyr Z , that in turn is reduced by the Mn 4 cluster. During the enzyme cycle, the oxidizing side of PSII goes through five different redox states that are denoted S n , n varying from 0 to 4.…”

“…Oxygen is released during the S 3 to S 0 transition in which S 4 is a transient state (reviewed in Refs. [1][2][3][4]. Ca 2ϩ ions are known to be required for enzyme activity (1,(5)(6)(7)(8).…”

Functional models for the oxygen-evolving complex of photosystem II

“…Decades of biophysical study have provided a solid groundwork for this project. Crystal structures of photosystem II [1,2] (PSII) have revealed the location of many important components such as chlorophylls and the oxygen-evolving center (OEC) while spectroscopy such as EXAFS [3][4][5][6][7], EPR [8][9][10][11][12], and IR [13,14] have allowed the study of reactive intermediates, the composition of the OEC and the protein ligation of the metal centers. Unfortunately, while we now have a much better structural and mechanistic basis for PSII, we still are some way from the goal of a molecular mechanistic understanding of water oxidation.…”

Absence of Mn-Centered Oxidation in the S2 → S3 Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

“…The conflicting results in the literature concerning the S 2 → S 3 transition, some of which support and some of which disagree with Mn oxidation occurring during this transition, have led to two different types of proposed O 2 evolution mechanisms, with one type 8,[10][11][12]15,16 incorporating the oxidation of ligand or substrate in the S 3 state, and the other type 9,13,54 invoking Mn oxidation during the S 2 → S 3 transition. As expected, fundamental differences in the chemistry of O-O bond formation and O 2 evolution exist between the two types of mechanisms.…”