Mechanism of Intramolecular Electron Transfer in the Photoexcited Zn-Substituted Cytochrome c: Theoretical and Experimental Perspective

• Published in: Journal of the American Chemical Society Vol. 130; no. 15; pp. 5302 - 5310
• Main Authors: Tokita, Yuichi, Shimura, Jusuke, Nakajima, Hiroshi, Goto, Yoshio, Watanabe, Yoshihito
• Format: Journal Article
• Language: English
• Published: United States American Chemical Society 16.04.2008
• Subjects: Animals; Cytochromes c - chemistry; Cytochromes c - metabolism; Electrodes; Electron Transport; Gold - chemistry; Horses; Models, Molecular; Molecular Conformation; Photochemistry; Porphyrins - chemistry; Porphyrins - metabolism
• ISSN: 0002-7863; 1520-5126
• DOI: 10.1021/ja711324t

Photoinduced electron transfer (ET) in zinc-substituted cytochrome c (Zn-cyt c) has been utilized in many studies on the long-range ET in protein. Attempting to understand its ET mechanism in terms of electronic structure of the molecule, we have calculated an all-electron wave function for the ground-state of Zn-cyt c on the basis of density functional theory (DFT). The four molecular orbitals (MOs) responsible for excitation by UV–vis light (Gouterman’s 4-orbitals) are assigned on the basis of the excited states of chromophore model for Zn−porphine complex calculated with the time-dependent DFT method. ET rates between each Gouterman’s 4-orbitals and other MOs were estimated using Fermi’s golden rule. It appeared that the two occupied MOs of the 4-orbitals show exclusively higher ET rate from/to particular MOs that localize on outermost amino acid residues (Lys 7 or Asn 54), respectively, whereas ET rates involving the two unoccupied MOs of the 4-orbitals are much slower. These results imply that the intramolecular ET in photoexcited Zn-cyt c is governed by the hole transfer through occupied MOs. The couplings of MOs between zinc porphyrin core and specific amino acid residues on the protein surface have been demonstrated in Zn-cyt c immobilized on an Au electrode via carboxylic acid group-terminated self-assembled monolayer. The Zn-cyt c-modified electrode showed photocurrents responsible for photoillumination. The action spectrum of the photocurrent was identical with the absorption spectrum of Zn-cyt c, indicating photoinduced electron conduction via occupied MOs. The voltage dependence of the photocurrent appeared to be linear and bidirectional like a photoconductor, which strongly supports the intramolecular ET mechanism in Zn-cyt c proposed on the basis of the theoretical calculations.