Elsevier

Chemical Physics Letters

Volume 627, 1 May 2015, Pages 44-52
Chemical Physics Letters

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On the guiding principles for lucid understanding of the damage-free S1 structure of the CaMn4O5 cluster in the oxygen evolving complex of photosystem II

https://doi.org/10.1016/j.cplett.2015.03.033Get rights and content

Highlights

  • Characteristic structural parameters in the oxygen evolving complex were examined.

  • A linear correlation between the Mna–Mnb and Mna–O5 distances was found.

  • Geometrical rules are important to elucidate the cluster structures and variations.

Abstract

Several key concepts and geometrical rules for the Mn–Mn and Mn–O distances of the CaMn4O5 cluster in the oxygen evolving complex (OEC) of photosystem II (PSII) by previous and present theoretical calculations were examined for a clear understanding of the damage-free S1 structure revealed by X-ray free electron laser (XFEL). A simple equation to estimate the Mna–Mnb distance in relation to the Mna–O(5) distance was derived taking into consideration the Jahn–Teller (JT) effects for Mn centers, indicating that the XFEL structure is regarded as a slightly right-elongated quasi-central structure in contradiction to a right-opened structure proposed by the EXAFS measurements.

Introduction

Photosystem II (PS II) is a large protein complex embedded in the thylakoid membranes of cyanobacteria, algae and plants, and is the only known biological system that has the unique capability of utilizing visible light for the oxidation of water into molecular oxygen as shown in Eq. (1) [1], [2]:2H2O + 4hν  O2 + 4e + 4H+.

The oxygen evolving complex (OEC) in PSII involves the active catalytic site which consists of four Mn ions and one Ca ion, namely the CaMn4O5 cluster. Molecular structures of the CaMn4O5 cluster in OEC of PSII from past decades have been investigated by the extended X-ray absorption fine structure (EXAFS) [3], [4], [5], [6], [7], [8], X-ray diffraction (XRD) [9], [10], [11], [12], [13], [14], [15], [16] and other experimental and theoretical methods. However, accumulated theoretical [17], [18], [19], [20], [21], [22], [23], [24], [25], [26] and experimental [27], [28], [29], [30], [31], [32] results have concluded that the high-resolution XRD structure analyzed with synchrotron X-rays [15] suffers from experimental uncertainty (about 0.16 Å) at 1.9 Å resolution and also possible structural damage induced by the strong X-ray radiation [5]. Over the last decade we performed quantum-mechanical (QM) and QM/MM calculations [33], [34], [35], [36], [37], [38], [39], [40], [41], [42], [43] of the CaMn4O5 cluster in OEC of PSII and elucidated general trends for the optimized Mn–Mn, Ca–Mn and Mn–O distances to account for the characteristic features of the structures obtained by XRD, EXAFS and several theoretical models.

Very recently Suga, Akita and Shen and their collaborators [16] performed the X-ray free electron laser (XFEL) experiments [27], [28], [29], [30], [31], [32] of PSII and obtained a radiation damage-free XRD structure of the dark stable S1 state of PSII by using the femtosecond X-ray pulses of XFEL provided by at the SPring-8 angstrom compact free-electron laser (SACLA) facility [32] and a huge number of highly isomorphous large crystals. The new XFEL structure at 1.95 Å resolution [16] was found to be different from the right-opened (R) structure (see Figure 1) based on previous theoretical [17], [18], [19], [20], [21], [22], [23], [24], [25], [26] computations. Alternatively the XFEL structure was topologically similar to the high-resolution XRD structure [15] that was suggestd to be X-ray damaged on the experimental [27], [28], [29], [30], [31], [32] grounds. Thus the XFEL results [16] raised a fundamental question, namely how to understand the geometrical structure of the CaMn4O5 cluster, indicating the necessity of re-examination of assumptions employed for several theoretical model structures of OEC of PSII, and also for re-examinations of the EXAFS structures [3], [4], [5], [6], [7], [8] reported previously.

In this paper we elucidate the guiding principles and basic assumptions to obtain theoretical structures of the CaMn4O5 cluster of OEC of PSII by DFT computations [17], [18], [19], [20], [21], [22], [23], [24], [25], [26], [33], [34], [35], [36], [37], [38], [39], [40], [41], [42]. To this end, we first investigate three important factors determining geometrical structures of the CaMn4O5 cluster: (1) structural symmetry breaking (SSB) of a labile Mna–X(5)–Mnd bond, (2) oxidation states of coordinated water molecule, namely OH or O2− at the X(5) = O(5) site and (3) Jahn–Teller effect for the Mn(III)a ion. The degrees of SSB of the labile Mna–X(5)–Mnd bond of the CaMn4O5 cluster elucidated by QM and QM/MM calculations indicate a slightly right-elongated quasi-central structure for XFEL, providing a simple semi-empirical equation for estimation of the Mna–Mnb and Mnd–O(5) distances in relation to the Mna–O(5) bond length. Implications of the computational results are discussed in relation to the understanding of the geometrical structure of the CaMn4O5 cluster, possible re-assignment of the EXAFS bond lengths to reproduce the XFEL structure [16] and elucidation of the scope and applicability of theoretical models proposed by several groups [17], [18], [19], [20], [21], [22], [23], [24], [25], [26].

Section snippets

Labile nature of the Mna–X(5)–Mnb bond in the CaMn4O5 cluster

Our broken-symmetry (BS) DFT computations [33], [34], [35], [36], [37], [38], [39], [40], [41], [42], [43] based on several quantum mechanical (QM) and QM/molecular mechanics (MM) models for OEC of PSII elucidated the labile nature of the Mna–X(5)–Mnb bond (X = H2O, OH, or O) of the CaMn4O5 cluster, providing four different geometrical structures as illustrated in Figure 1. The Mna–O(5) and Mnd–O(5) distances revealed by the high-resolution XRD structure (3ARC in the PDB) [15] were 2.50 and 2.60

QM and QM/MM calculations for the CaMn4O5 cluster

Past four years the discrepancy between XRD (3ARC and 3WU2) [15] and EXAFS structures [4], [6] has been extensively discussed [17], [18], [19], [20], [21], [22], [23], [24], [25], [26], suggesting two possibilities [37], [41], [42], namely (1) the experimental uncertainty (about 0.16 Å) and (2) the damage of the XRD structure induced by the strong X-ray radiation [5], [17], [18], [19], [20], [21], [22], [23], [24], [25], [26]. Detailed analysis of several theoretical models supporting the latter

Possible explanations of the EXAFS results

Past decades a number of EXAFS experiments [3], [4], [5], [6], [7], [8] were conducted for determination of the Mn–Mn and Ca–Mn distances in the CaMn4O5 cluster, concluding that there are two Mn–Mn distances at about 2.7 Å and one Mn–Mn distance at the 2.8 Å. However, the EXAFS experiments by the Berkeley group [5], [8] could not provide a unique 3D structure, suggesting several possible 3D structures as illustrated in Figure S3. The semi-empirical Eqs. (4a), (4b) provide the re-assigned Mn–Mn

Acknowledgements

Numerical calculations of the present work were carried out under the support of a Grants-in-Aid for Specially Promoted Research (No. 24000018) from MEXT, Japan.

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