[[The]] tuning of electron and proton-coupled electron transfer reactions of solar water oxidation : pulsed magnetic resonance spectroscopy studies of Photosystem II

Abstract

From analysis of the interactions of electron and proton transport cofactors the interaction of these cofactors with their surrounding environments through hydrogen bonding has been highlighted as a key interaction. Unlike previous accounts on electron transport dependence purely on the strength or length of a hydrogen bond between cofactor and protein, these studies put in a new light the dependence on hydrogen bond partner angular orientation to one another as a key tuning factor in the electron and proton transfer reactions with photosynthetic reaction centers.

In the photosynthetic reaction centers, Photosystem II (PSII) and Photosystem I (PSI), specific cofactors allow for the highly efficient electron and proton transfer through these proteins. While high-resolution X-ray crystal structures of both PSII and PSI have been published recently, there is limited information on the electronic structure of these charge-transfer cofactors. We have applied the magnetic resonance spectroscopy techniques of electron paramagnetic resonance (EPR) spectroscopy and solid state nuclear magnetic resonance (NMR) spectroscopy to the analysis of electron transport cofactors of photosynthetic reaction centers. The electronic and molecular structure of photosynthetic electron transport cofactors have been probed in two distinct effects 1) internal effects on structure through cofactor functional group substitution, and 2) external effects on structure through interaction with cofactor environment (electrostatics, π-stacking, hydrogen bonding, hydrophobicity). A detailed description of the tuning of photosynthetic electron transport cofactors by their protein environments will help facilitate the design of more efficient, bio-inspired solar energy capture systems.

The highly demanding reaction of water oxidation occurs at the donor-side of PSII. This reaction takes place at the tetranuclear manganese-calcium-oxo (Mn4-Ca-oxo) cluster that is facilitated by the proton-coupled electron transfer (PCET) reactions at a redox-active tyrosine residue (YZ). PSII contains two symmetric tyrosine residues, YZ and YD, within the heterodimeric polypeptide core, which though chemically identical display very different redox and kinetic properties. On the donor-side of PSII, I use pulsed EPR on, 1) effects of the ligand environment and small molecule coordination on the electronic structure of the Mn4-Ca-oxo cluster and the proteinaceous model, manganese catalase, and 2) the electronic properties of the local environments of YZ and YD to obtain insight on the functional tuning of PCET reactions of these two redox-active tyrosine residues.

On the acceptor side of PSII and in the cofactor chain of PSI, quinones function as electron transport cofactors. The versatility and functional diversity of quinone cofactors is primarily due to the diverse mid-point potentials that are tuned by the substituent effects and interactions with surrounding amino acids residues in their respective protein binding pockets. I demonstrate the use of pulsed EPR spectroscopy to describe: 1) an analysis of a library of substituted 1,4 naphthoquinone molecules to correlate the mid-point potentials with the electronic structure, 2) the effects of site-specific mutagenesis on the electron structure of the electron acceptor, QA, of PSII, and 3) the electronic structure of substituted neutral radical hydroquinones and their relation to the PCET reactions of photosynthetic chemical energy storage. I also demonstrate the analysis of a library of substituted benzoquinone molecules by solid-state NMR and demonstrate its potential use in determining quinone-protein interactions.