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 (Q _A ) to secondary (Q _B ) 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 Q _A → Q _B 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 Q _A and Q _B . 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. Fe ²⁺ is not an essential component for the Q _A → Q _B electron tunneling because hybridized histidine molecular orbitals can be coupled with both Q _A and Q _B simultaneously in the absence of Fe d orbitals.