Long-Range Interaction between the Mn4CaO5 Cluster and the Non-heme Iron Center in Photosystem II as Revealed by FTIR Spectroelectrochemistry

It is known that inactivation of the Mn4CaO5 cluster, the catalytic center of water oxidation in photosystem II (PSII), induces a positive shift of the redox potential (E-m) of the primary quinone electron acceptor Q(A) by similar to+150 mV, resulting in suppression of the electron transfer from QA to the secondary quinone acceptor Q(B). Although the relevance of this E-m(Q(A)(-)/Q(A)) shift to the photoprotection of PSLT has been debated, its molecular mechanism is still enigmatic from a structural viewpoint because Q(A) is similar to 40 angstrom from the Mn4CaO5 cluster. In this work, we have investigated the influence of Mn depletion on the E-m of the non-heme iron, which is located between Q(A) and Q(B), and its surrounding structure. Electrochemical measurements in combination with Fourier transform infrared (FTIR) spectroscopy revealed that Mn depletion shifts E-m(Fe2+/Fe3+) by +18 mV, which is similar to 8 times smaller than the shift of E-m(Q(A)(-)/Q(A)). Comparison of the Fe2+/Fe3+ FTIR difference spectra between intact and Mn-depleted PSII samples showed that Mn depletion altered the pK(a)'s of a His ligand to the non-heme iron, most probably the D1-His215 interacting Q(B), and a carboxylate group, possibly D1-Glu244, coupled with the non-heme iron. It was further shown that Mn depletion influences the C equivalent to N vibration of bromoxynil bound to the Q(B) site, indicative of the modification of the Q(B) binding site. On the basis of these results, we discuss the mechanism of a long-range interaction between the donor and acceptor sides of PSII.