Both electronic and vibrational coherences are involved in primary electron transfer in bacterial reaction center

Fei Ma,Vladimir I Novoderezhkin,Elisabet Romero,Michael R Jones,Rienk Van Grondelle

doi:10.1038/s41467-019-08751-8

Fei Ma, Vladimir I Novoderezhkin + Show 3 more

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https://doi.org/10.1038/s41467-019-08751-8

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Abstract

Understanding the mechanism behind the near-unity efficiency of primary electron transfer in reaction centers is essential for designing performance-enhanced artificial solar conversion systems to fulfill mankind’s growing demands for energy. One of the most important challenges is distinguishing electronic and vibrational coherence and establishing their respective roles during charge separation. In this work we apply two-dimensional electronic spectroscopy to three structurally-modified reaction centers from the purple bacterium Rhodobacter sphaeroides with different primary electron transfer rates. By comparing dynamics and quantum beats, we reveal that an electronic coherence with dephasing lifetime of ~190 fs connects the initial excited state, P*, and the charge-transfer intermediate {mathrm{P}}_{mathrm{A}}^ + {mathrm{P}}_{mathrm{B}}^ -; this {mathrm{P}}^ ast to {mathrm{P}}_{mathrm{A}}^ + {mathrm{P}}_{mathrm{B}}^ - step is associated with a long-lived quasi-resonant vibrational coherence; and another vibrational coherence is associated with stabilizing the primary photoproduct, {mathrm{P}}^ + {mathrm{B}}_{mathrm{A}}^ -. The results show that both electronic and vibrational coherences are involved in primary electron transfer process and they correlate with the super-high efficiency.

Highlights

Understanding the mechanism behind the near-unity efficiency of primary electron transfer in reaction centers is essential for designing performance-enhanced artificial solar conversion systems to fulfill mankind’s growing demands for energy
To distinguish electronic and vibrational coherence and identify their respect roles, in this work we extend our previous study by analyzing two double-site mutant Reaction centers (RCs) that exhibit slowed primary electron transfer (ET) rates in addition to the QA-excluding AM260W mutation. 2DES experiments are conducted at 77 K rather than the room temperature used in our previous work, producing more distinguishable spectral shapes and revealing shortlived intermediates that are usually hidden in a room-temperature experiment
Using 2DES, we surprisingly found that charge separation in M2 did not involve BA was tmhue cPhþAsPloÀBwinerteartm(e2d6i0atpes)C−T1.sTtahtee, and direct reason for ET the from P* absence to of a PþA PÀB state may be that the relative configurations of PA and PB

Summary

Introduction

Understanding the mechanism behind the near-unity efficiency of primary electron transfer in reaction centers is essential for designing performance-enhanced artificial solar conversion systems to fulfill mankind’s growing demands for energy. By comparing dynamics and quantum beats, we reveal that an electronic coherence with dephasing lifetime of ~190 fs connects the initial excited state, P*, and the charge-transfer intermediate PþA PÀB ; this PÃ ! The idea of quantum coherence playing a role in photosynthesis arose from observations that some energy or electron transfer processes in bacterial and plant pigment–protein complexes are efficient to an extent that exceeds explanation using only classical theory[1,2]. Since its first implementation[3], two-dimensional electronic spectroscopy (2DES) has become a powerful tool for the study of coherent mechanisms in photosynthetic complexes, with broadband excitation creating coherent superpositions of electronic/vibrational states that give rise to specific features in the 2D spectra such as quantum beats (QBs). Charge separation is initiated from the excited state of P (P*), forming a partial intradimer charge-transfer (CT) intermediate, PþA PÀB

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