Long-Range Electron Tunneling from the Primary to Secondary Quinones in Photosystem II Enhanced by Hydrogen Bonds with a Nonheme Fe Complex.

The mechanisms governing the long-range electron tunneling from the primary (QA) to secondary (QB) quinones in photosystem II are clarified by analyzing superexchange pathways through a nonheme Fe complex, using a quantum mechanics/molecular mechanics/polarizable continuum model approach. The electron tunneling rate is evaluated using the Marcus-Levich-Jortner theory considering electronic coupling, energy difference, and Franck-Condon factor. The superexchange QA → QB electron tunneling is enhanced by hybridized σ/σ* orbitals of histidines (D2-His214 and D1-His215) via penetration of the wave function into hydrogen bonds with both QA and QB. Despite a large energy gap to the intermediate states, the contributions of the histidine σ/σ* orbitals to the superexchange coupling are larger than those of π/π* orbitals. Fe2+ is not an essential component for the QA → QB electron tunneling because hybridized histidine molecular orbitals can be coupled with both QA and QB simultaneously in the absence of Fe d orbitals.