21 research outputs found
Fourier Transform Infrared Detection of a Polarizable Proton Trapped between Photooxidized Tyrosine Y<sub>Z</sub> and a Coupled Histidine in Photosystem II: Relevance to the Proton Transfer Mechanism of Water Oxidation
The redox-active tyrosine Y<sub>Z</sub> (D1-Tyr161) in photosystem
II (PSII) functions as an immediate electron acceptor of the Mn<sub>4</sub>Ca cluster, which is the catalytic center of photosynthetic
water oxidation. Y<sub>Z</sub> is also located in the hydrogen bond
network that connects the Mn<sub>4</sub>Ca cluster to the lumen and
hence is possibly related to the proton transfer process during water
oxidation. To understand the role of Y<sub>Z</sub> in the water oxidation
mechanism, we have studied the hydrogen bonding interactions of Y<sub>Z</sub> and its photooxidized neutral radical Y<sub>Z</sub><sup>•</sup> together with the interaction of the coupled His residue, D1-His190,
using light-induced Fourier transform infrared (FTIR) difference spectroscopy.
The Y<sub>Z</sub><sup>•</sup>-minus-Y<sub>Z</sub> FTIR difference
spectrum of Mn-depleted PSII core complexes exhibited a broad positive
feature around 2800 cm<sup>–1</sup>, which was absent in the
corresponding spectrum of another redox-active tyrosine Y<sub>D</sub> (D2-Tyr160). Analyses by <sup>15</sup>N and H/D substitutions, examination
of the pH dependence, and density functional theory and quantum mechanics/molecular
mechanics (QM/MM) calculations showed that this band arises from the
N–H stretching vibration of the protonated cation of D1-His190
forming a charge-assisted strong hydrogen bond with Y<sub>Z</sub><sup>•</sup>. This result provides strong evidence that the proton
released from Y<sub>Z</sub> upon its oxidation is trapped in D1-His190
and a positive charge remains on this His. The broad feature of the
∼2800 cm<sup>–1</sup> band reflects a large proton polarizability
in the hydrogen bond between Y<sub>Z</sub><sup>•</sup> and
HisH<sup>+</sup>. QM/MM calculations further showed that upon Y<sub>Z</sub> oxidation the hydrogen bond network is rearranged and one
water molecule moves toward D1-His190. From these data, a novel proton
transfer mechanism via Y<sub>Z</sub><sup>•</sup>-HisH<sup>+</sup> is proposed, in which hopping of the polarizable proton of HisH<sup>+</sup> to this water triggers the transfer of the proton from substrate
water to the luminal side. This proton transfer mechanism could be
functional in the S<sub>2</sub> → S<sub>3</sub> transition,
which requires proton release before electron transfer because of
an excess positive charge on the Mn<sub>4</sub>Ca cluster