S1-state Mn4Ca complex of Photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence

摘要

Photosynthetic water oxidation reaction driven by Sun and catalyzed by a unique Mn4Ca 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 Thermosyn-echococcus vulcanus was resolved by 1.9 A-resolution XRD data [55]. Interestingly, it revealed an unusual oxo-bridged Mn4CaO5 cluster in the dark stable S1-state, e.g. unusual mono-μ2-oxo-mono-μ4-oxo-mono-μ2-carboxylato bridges connecting Mn_a (terminal) and Mn_b (central) ions with unusual atomic distance of 2.9 A. 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 S1 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 Mn4Ca clusters in S_(1a) and S_(1b) are given by R_(ab) = 3.32 A and 2.77 A, respectively, so that the apparent distance between Mn_a and Mn_b ions in isomeric equilibrium is given by 2.94 A, in agreement with experimental R_(ab) ~ 2.9 A. Concomitantly, the first full-k-range EXAFS spectrum from powdered PSII [45] is used to provide the second experimental evidence for the S1-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 Mn4Ca 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 S1 by time-resolved ~(18)O-exchange mass spectroscopy.