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

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 [Formula: see text]; this [Formula: see text] step is associated with a long-lived quasi-resonant vibrational coherence; and another vibrational coherence is associated with stabilizing the primary photoproduct, [Formula: see text]. The results show that both electronic and vibrational coherences are involved in primary electron transfer process and they correlate with the super-high efficiency.

Fig. 1

Cofactor structure and absorption spectra of reaction centers (RCs). a Arrangement of cofactors and the electron transfer (ET) pathway in M1, which lacks a Q_A acceptor due to an alanine to tryptophan replacement (the crystal structure is from PDB record 1QOV). b Normalized absorption spectra of M1 (solid line), M2 (dashed line), and M3 (light solid line) at 77 K overlaid with the laser spectrum (gray shaded area). c Scheme of charge separation (pink arrow) and ET (black arrow) with mutation site for M2 (Tyr M210, purple) and M3 (Gly M203, red). A water molecule (gray ball) links P_B and B_A via a hydrogen-bond interaction involving the former’s axial histidine M202 (dotted lines)

Fig. 2

77 K absorptive total two-dimensional (2D) spectra. 2D spectra of M1 (a), M2 (b), and M3 (c). Symbols λ_τ and λ_t denote the excitation and detection wavelengths, respectively; the indicated population time T is shown in the left-top corner of each panel. The spectra are normalized to the maximum of the diagonal P signal; the relative amplitude multiplier is shown below the T

Fig. 3

Two-dimensional evolution-associated spectra (2D-EAS). 2D-EAS of M1 (a), M2 (b), and M3 (c). The time constants of each species are shown in the left-top corner of each panel. The spectra are normalized to the maximum of the diagonal P signal; the relative amplitude multiplier is shown below the time constants. The crosses in each component-2 EAS mark the approximate location of the $\left({\mathrm{P}}^{*}\mathrm{,}{\mathrm{P}}_{\mathrm{A}}^{+}{\mathrm{P}}_{\mathrm{B}}^{-}\right)$ cross peak

Fig. 4

Quantum beats and Fourier transform (FT) power spectra. The top, middle, and bottom traces represent M1, M2, and M3. a Real-part T traces at the cross-peak locations as labeled with a cross in Fig. 3 after subtraction of multiexponential dynamics. b Summary FT power spectra of the oscillations in the real-part signals (0–2 ps)

Fig. 5

Coherent primary electron transfer. A scheme of the primary electron transfer process facilitated by coherences