Structural and energetic insights into Mn-to-Fe substitution in the oxygen-evolving complex

Abstract

Manganese (Mn) serves as the catalytic center for water splitting in photosystem II (PSII), despite the abundance of iron (Fe) on earth. As a first step toward why Mn and not Fe is employed by Nature in the water oxidation catalyst, we investigated the Fe₄CaO₅ cluster in the PSII protein environment using a quantum mechanical/molecular mechanical (QM/MM) approach, assuming an equivalence between Mn(III/IV) and Fe(II/III). Substituting Mn with Fe resulted in the protonation of μ-oxo bridges at sites O2 and O3 by Arg357 and D1-His337, respectively. While the Mn₄CaO₅ cluster exhibits distinct open- and closed-cubane S₂ conformations, the Fe₄CaO₅ cluster lacks this variability due to an equal spin distribution over sites Fe1 and Fe4. The absence of a low-barrier H-bond between a ligand water molecule (W1) and D1-Asp61 in the Fe₄CaO₅ cluster may underlie its incapability for ligand water deprotonation, highlighting the relevance of Mn in natural water splitting.

Keywords: Catalysis; Chemistry; Photoabsorption.

Graphical abstract

Figure 1

Protonation state of CP43-Arg357 and D1-His337 and overview of the clusters (A) Fe₄CaO₅ cluster in Fe(II)Fe(III)₃. (B) Mn₄CaO₅ cluster in Mn(III)Mn(IV)₄ (open-cubane S₂ conformation). (C) Overview of the Fe₄CaO₅ cluster. (D) Overview of the Mn₄CaO₅ cluster. Only H atoms of CP43-Arg357 and D1-His337 are explicitly shown (black ball) for clarity. The black thick arrow indicates the protonation event. Red arrows indicate movement of protons during QM/MM calculations.

Figure 2

Potential energy profile for the O5 position along the Fe1 … O5 … Fe4 and Mn1 … O5 … Mn4 axes (A) Fe₄CaO₅ cluster. (B) Mn₄CaO₅ cluster. In the Mn₄CaO₅ cluster, the global energy minimum corresponds to the open-cubane S₂ conformation, whereas the local energy minimum corresponds to the closed-cubane S₂ conformation.

Figure 3

Potential energy profile for the H-bond between H₂O at W1 and D1-Asp61 (A) Fe₄CaO₅ cluster. (B) Mn₄CaO₅ cluster. Labels W1 and Asp61 indicate the W1 and D1-Asp61 moieties in the H-bond, respectively.

Figure 4

H-bond network of the Fe₄CaO₅ and Mn₄CaO₅ clusters (A) H-bond network of TyrZ for the Fe₄CaO₅ cluster. (B) H-bond network of TyrZ for the Mn₄CaO₅ cluster (open-cubane S₂ conformation). (C) H-bond network near the Cl-1 binding site for the Fe₄CaO₅ cluster. (D) H-bond network near the Cl-1 binding site for the Mn₄CaO₅ cluster (open-cubane S₂ conformation). Dotted lines indicate H-bonds.

Figure 5

Potential energy profile for the H-bond between TyrZ and D1-His190 (A) Fe₄CaO₅ cluster. (B) Mn₄CaO₅ cluster. Labels TyrZ and His190 indicate the TyrZ and D1-His190 moieties in the H-bond, respectively. Although the shape of the potential-energy curve for the TyrZ … His190 of the Mn₄CaO₅ cluster (B) resembles that for the W1 … D1-Asp61 of the Mn₄CaO₅ cluster (Figure 3B) due to low-barrier H-bonds, the numerical data are different.