Reversible Structural Isomerization of Nature's Water Oxidation Catalyst Prior to O-O Bond Formation

Abstract

Photosynthetic water oxidation is catalyzed by a manganese-calcium oxide cluster, which experiences five "S-states" during a light-driven reaction cycle. The unique "distorted chair"-like geometry of the Mn₄CaO₅₍₆₎ cluster shows structural flexibility that has been frequently proposed to involve "open" and "closed"-cubane forms from the S₁ to S₃ states. The isomers are interconvertible in the S₁ and S₂ states, while in the S₃ state, the open-cubane structure is observed to dominate inThermosynechococcus elongatus (cyanobacteria) samples. In this work, using density functional theory calculations, we go beyond the S₃⁺Y_z state to the S₃ⁿY_z^• → S₄⁺Y_z step, and report for the first time that the reversible isomerism, which is suppressed in the S₃⁺Y_z state, is fully recovered in the ensuing S₃ⁿY_z^• state due to the proton release from a manganese-bound water ligand. The altered coordination strength of the manganese-ligand facilitates formation of the closed-cubane form, in a dynamic equilibrium with the open-cubane form. This tautomerism immediately preceding dioxygen formation may constitute the rate limiting step for O₂ formation, and exert a significant influence on the water oxidation mechanism in photosystem II.

Figure 1

(a) View of PSII dimer and the OEC location from Thermosynechococcus elongatus (PDB ID: 6W1O) (b) Mn₄CaO₅ cluster and its local surroundings in its dark-stable S₁ state. (c) Sketch map of atom labeling and connectivity of the first coordination sphere ligands in the Mn₄CaO₅ cluster. (d) Extended S-state cycle including nine intermediates with sequence of proton and electron transfer and kinetics between transitions;^,−,,,, the red phase is the main focus of this study. (e) Structural flexibility of the OEC cluster in the S₁, S₂, and S₃ states, marked with the reversibility between open (A) and closed (B) cubane structures (for references, see the main text).

Scheme 1. Structural Isomerization between S₃^A,WY_z^• (Left) and S₃^B,WY_z^• (Right) in the S₃ⁿY_z^• (W1 = OH^–) State Explored in the Present Study

Amino acid ligands are omitted for clarity.

Figure 2

(a) Relative Gibbs free energy profiles for the conversion between S₃^A,WY_z(W1=H₂O) and S₃^B,WY_z(W1=H₂O) in all the possible spin states of the S₃⁺Y_z state. Because of the close similarity to the other spin states, more information regarding the changes of (b) geometric structures, (c) electronic configurations along the MEP, and (d) relaxed PES scan curve of proton transfer between Ox and O5 are exemplified in the highest 13-et/αααα spin state. Spin populations are displayed in yellow contours and key interatomic distances are given in Å.

Figure 3

(a) Relative Gibbs free energy profiles for the conversion between S₃^A,WY_z^•(W1=OH^–) and S₃^B,WY_z^•(W1=OH^–) in all the possible spin states of the S₃ⁿY_z^• state. Because of the close similarity to the other spin states, the highest 14-et/ααααα spin state was selected for visualizing more information regarding the changes of (b) geometric structures and (c) electronic configurations along the MEP, and (d) relaxed PES scan curve of proton transfer between Ox and O5.

Figure 4

Relative Gibbs free energy profiles for the conversions between the virtual states S₃^A,WY_z^•(W1=H₂O)* and S₃^B,WY_z^•(W1=H₂O)* (left) and between the virtual states S₃^A,WY_z(W1=OH^–)* and S₃^B,WY_z(W1=OH^–)* (right) in their respective highest spin states; “*” denotes a virtual state.

Scheme 2. Possible mechanisms of the S₃ → S₄ transition and O–O Bond formation in the S₄ State

S₃^A,W and S₃^B,unbound in gray stand for the two potential starting configurations in the S₃ state, resolved in cyanobacteria and higher-plant PSII by XFEL and EPR experiments, respectively.^−,, The process focused in this work is highlighted in the green dashed box. Candidate substrates are encircled in red (favored) or blue (possible alternatives). Mn formal oxidation states (IV)(V) are displayed in different colors. The superscript “W”/“unbound” means hexa/penta-coordinate Mn4 with a water bound/unbound water trans to O5. The annotations for sequence numbers: (a,g) Y_z oxidation followed by proton release; (b,d,h) intramolecular proton transfer followed by Ox/W2/O5/Mn4 oxidation; (c) reversible open-closed rearrangement in the S₃ⁿY_z^● state, as proposed in this study; (e,i) reversible water binding to the five-coordinate Mn4(IV) in the closed-cubane structure; and (f) irreversible closed-to-open conversion in the S₃ state. Other proposed mechanisms are discussed in the text. It is noted that the oxygen labeling for S₃^B,W and S₃^B,unbound (and their derivatives) is chosen for consistency with that established by serial crystallography for the S₃^A,W,, and for convenience to describe all the transitions uniformly. These labels do not reflect the origin of the oxygens with regard to the S₁ and S₂ states because several options for water insertion during the S₂ → S₃ transition are still discussed;^{,,,,,,,,,,,−} an alternative nomenclature based on S₃^B,unbound and the pivot/carousel water insertion is shown in Figure S4 in the Supporting Information.