PCET IN GROTTHUSS-TYPE PROTON WIRES: THERMODYNAMICS, DYNAMICS, AND BIOHYBRIDS

Resumen

Proton-coupled electron transfer (PCET) is the transfer of an electron from one site to another accompanied by the transfer of proton/s. PCET and the transport of protons over tens of angstroms are essential to bioenergetics in all living cells because they are a fundamental link between redox processes and the generation of transmembrane gradients of proton potential, known as proton-motive force (PMF). Inspired by the PCET process in photosystem II involving Tyrz-His190, we and others have used a benzimidazole-phenol (BIP) system to illustrate an E1PT process, where one-electron oxidation of the phenol is accompanied by the transfer of its proton to the attached benzimidazole.1 With amino- and other-substituted BIPs, we showed that one-electron, two-proton (E2PT) PCET reactions occur.2 Aiming at long-range proton translocation, we designed constructs capable of Grotthuss-type proton translocation consisting of a phenol, a polybenzimidazole hydrogen-bond network, and a terminal proton acceptor (TPA). These “proton wires” translocates protons up to ∼16 Å by an E4PT process.3
To initiate an E1PT process photochemically, we designed a BIP covalently attached to a tripentafluorophenylporphyrin (BIPPF15). Studies of BIPPF15 by two-dimensional electronic-vibrational spectroscopy (2DEV) showed that PCET takes place on two-time scales: 1) an ultrafast process from the unrelaxed S1 state, and 2) a slower process competing with fluorescence from the relaxed S1 state. The ultrafast process enabled us to observe the evolution of the initial excited state to full charge separation as evidenced by the development of a dipole moment upon dihedral twisting between the BIP and the macrocycle on the 120 fs time scale.4 The dynamics of a photoinduced E2PT process were explored by substituting the BIP of BIPPF15 by a pyridine derivative TPA. We found that following porphyrin excitation, proton arrival on the TPA and electron arrival on the porphyrin are concerted to within 24 fs.5
Our next aim is to study PCET in protein environments. In preparation for this, a hybrid construct consisting of a four-helix bundle enclosing a Mn-porphyrin (Mn(II)-Por) docked to a high potential bacterial reaction center (BRC) was assembled. Exciting the BRC at 865 nm reversibly oxidizes Mn(II)-Por to Mn(III)-Por, demonstrating that the BRC communicates in a redox process with the Mn-porphyrin. This is a promising result for the idevelopment of hybrid artificial photosynthetic constructs in which energy-conserving processes could be reengineered and optimized.
References
1) Mora, S. J. et al. Acc. Chem. Res. 2018, 51 (2), 445-453.
2) Odella, E. et al. J. Am. Chem. Soc. 2018, 140 (45), 15450-15460.
3) Odella, E. et al. J. Am. Chem. Soc. 2019, 141 (36), 14057-14061.
4) Yoneda, Y. et al. J. Am. Chem. Soc. 2021, 143 (8), 3104-3112.
5) Arsenault, E. A. J. Phys. Chem. Lett. 2022, 13 (20), 4479-4485.