Understanding Two Different Structures in the Dark Stable State of the Oxygen‐Evolving Complex of Photosystem II: Applicability of the Jahn–Teller Deformation Formula

Abstract

Tanaka et al. (J. Am. Chem. Soc., 2017, 139, 1718) recently reported the three‐dimensional (3D) structure of the oxygen evolving complex (OEC) of photosystem II (PSII) by X‐ray diffraction (XRD) using extremely low X‐ray doses of 0.03 and 0.12 MGy. They observed two different 3D structures of the CaMn4O5 cluster with different hydrogen‐bonding interactions in the S1 state of OEC keeping the surrounding polypeptide frameworks of PSII the same. Our Jahn–Teller (JT) deformation formula based on large‐scale quantum mechanics/molecular mechanics (QM/MM) was applied for these low‐dose XRD structures, elucidating important roles of JT effects of the MnIII ion for subtle geometric distortions of the CaMn4O5 cluster in OEC of PSII. The JT deformation formula revealed the similarity between the low‐dose XRD and damage‐free serial femtosecond X‐ray diffraction (SFX) structures of the CaMn4O5 cluster in the dark stable state. The extremely low‐dose XRD structures were not damaged by X‐ray irradiation. Implications of the present results are discussed in relation to recent SFX results and a blue print for the design of artificial photocatalysts for water oxidation.

Structural isomers of the S2 state in photosystem II: do they exist at room temperature and are they important for function?

“…For example, the importance of the spin isomorphism observed in the S 2 state has been suggested in recent studies (Pantazis et al 2012, Isobe et al 2014, in relation to the formation of the S 3 state, where the chemical environment is prepared for the O-O bond formation to occur in the following steps. Similarly, there have been suggestions of isomorphism in the S 1 (S total = 0 and S total = 1) and S 3 states (S total = 3 and an undetermined higher spin state that is not detected by EPR), all of which are detected under cryogenic temperatures (Boussac et al 2009, Isobe et al 2014, Shoji et al 2018. The presence and population of the isomers in each S-state under physiological conditions remains to be established.…”

Linear Response Functions of Densities and Spin Densities for Systematic Modeling of the QM/MM Approach for Mono- and Poly-Nuclear Transition Metal Systems

“…This was often used for biochemical systems until the 1990s [52]. If the model satisfies the criterion, |δρ(r)/δv(J)| (and |δρz(r)/δvm(J)|)<0.01, it is consistent with almost all QM/MM modeling [5,50,51]. In order to satisfy the guidelines given by Equation (17), i.e., |δρ(r)/δv(J)| <0.01 and |δρz(r)/δvm(J)|<0.01, the next surrounding environments beyond the weakly coupled interconnections, such as hydrogen bonds and hyperconjugations over sp3 junction, should be included in the QM region.…”

“…This implies that the approximation of glutamic acid and aspartic acid residues, as formic acids, is not appropriate. In fact, many researchers model glutamic acid or aspartic acid residues as acetic acids [5,50,51]. Note that the isosurface for δρ(r)/δv(Mn(3))=±0.001 are slightly delocalized to the two sp3 junctions away, C(47) from the C(43)O(41)O(42) carboxylate, as shown in Figure S10.…”

“…On the other hand, the model that is constructed according to the guideline, δρ(I)/δv(J)<0.01, the core part is described with the correct surrounding effects such as hydrogen bonds and the hyperconjugation effects. In fact, almost all models that are employed by most QM/MM researchers seem to satisfy this criterion [5,6,7,8,9,10,11,12,13,14,15,16,17,50,51]. As shown Figure 15c, the criterion, δρ(I)/δv(J)<0.001, leads to a greater number of interaction islands, which interconnect among units, and so, in other words, it requires a large QM region.…”

“…However, we would like to emphasize again that, for estimating the correct stable spin states, the problem remains rather in the approximation of the exchange-correlation functional we used than how to model the system by the QM/MM method [53,55]. In the next section, we examine the specific spin state and oxidation state that were proposed to be as the ground state of the OEC core [50,51] to evade the issue, such as the performance of the XC functional for estimating the relative stability among many degenerate states. In other words, we focus our attention only on the errors of densities and spin densities from the full QM model, which is given by Figure 11 in this study.…”