S 1-state Mn 4Ca complex of Photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence

Abstract

Photosynthetic water oxidation reaction driven by Sun and catalyzed by a unique Mn 4Ca cluster in Photosystem II (PSII) is known to take place in an oxygen evolving complex (OEC) that cycles five serial redox states, named “Kok’s S i -states” ( i = 0–4). Recently, the atomic crystal structure of PSII from Thermosynechococcus vulcanus was resolved by 1.9 Å-resolution XRD data [55]. Interestingly, it revealed an unusual oxo-bridged Mn 4CaO 5 cluster in the dark stable S 1-state, e.g. unusual mono-μ 2-oxo-mono-μ 4-oxo-mono-μ 2-carboxylato bridges connecting Mn a (terminal) and Mn b (central) ions with unusual atomic distance of 2.9 Å. Using the UDFT/B3LYP/lacvp ∗∗ geometry optimization method and a truncated cluster model of the chemically-complete OEC put in ε = 4 dielectric medium, it is shown that the OEC in S 1 must be in thermal equilibrium between the most-stable isomeric substates (“S 1a and S 1b”) owing to the quasi-reversible structure change induced by proton migration. Coincidentally, it is found that the Mn a–Mn b distances in the Mn 4Ca clusters in S 1a and S 1b are given by R ab = 3.32 Å and 2.77 Å, respectively, so that the apparent distance between Mn a and Mn b ions in isomeric equilibrium is given by 2.94 Å, in agreement with experimental R ab ∼ 2.9 Å. Concomitantly, the first full- k-range EXAFS spectrum from powdered PSII [45] is used to provide the second experimental evidence for the S 1-state OEC being in thermal equilibrium between S 1a and S 1b-isomers. These OEC-isomers consist of all the chemically-essential 11 amino acid residues, six cofactor ions and nine essential hydrated water molecules in their chemical ionic states around physiological pH 7, thus reasonably satisfying the biochemical charge neutrality with four Mn ions staying at the oxidation states ( Mn a III / Mn b IV / Mn c III / Mn d IV ) with the skeleton structures of MT-5J type and T-shaped DD-4J type. These H-bonding water molecules are found to fill a cavity connecting possible substrate/products channels so as to be arranged as an indispensable part of the catalytic Mn 4Ca cluster in the order of “current-substrates” (W1/W2 bound to Mn a III ), “next-substrates” (W4/W7) and “next–after-next-substrates” (W5/W6 bound to Ca 2+). Results show that the Jahn–Teller effect due to Mn a III ion in these isomers can reasonably explain the very-slow-exchange and very-fast-exchange processes observed in S 1 by time-resolved 18O-exchange mass spectroscopy.