Redox conditions correlated with vibronic coupling modulate quantum beats in photosynthetic pigment-protein complexes

Abstract

Quantum coherences, observed as time-dependent beats in ultrafast spectroscopic experiments, arise when light-matter interactions prepare systems in superpositions of states with differing energy and fixed phase across the ensemble. Such coherences have been observed in photosynthetic systems following ultrafast laser excitation, but what these coherences imply about the underlying energy transfer dynamics remains subject to debate. Recent work showed that redox conditions tune vibronic coupling in the Fenna-Matthews-Olson (FMO) pigment-protein complex in green sulfur bacteria, raising the question of whether redox conditions may also affect the long-lived (>100 fs) quantum coherences observed in this complex. In this work, we perform ultrafast two-dimensional electronic spectroscopy measurements on the FMO complex under both oxidizing and reducing conditions. We observe that many excited-state coherences are exclusively present in reducing conditions and are absent or attenuated in oxidizing conditions. Reducing conditions mimic the natural conditions of the complex more closely. Further, the presence of these coherences correlates with the vibronic coupling that produces faster, more efficient energy transfer through the complex under reducing conditions. The growth of coherences across the waiting time and the number of beating frequencies across hundreds of wavenumbers in the power spectra suggest that the beats are excited-state coherences with a mostly vibrational character whose phase relationship is maintained through the energy transfer process. Our results suggest that excitonic energy transfer proceeds through a coherent mechanism in this complex and that the coherences may provide a tool to disentangle coherent relaxation from energy transfer driven by stochastic environmental fluctuations.

Keywords: excitonics; light harvesting; photosynthesis; quantum biology; ultrafast spectroscopy.

Fig. 1.

Redox condition affects excited-state behavior in the wild-type FMO complex. (A) Structure of the FMO complex and the eight bacteriochlorophyll a sites held by the protein scaffold (Protein Data Bank ID code 3ENI) (29). Shown in red are the two cysteine residues, C49 and C353, that are known to steer and quench excitations in oxidizing conditions and tune vibronic coupling for enhanced energy transfer in reducing conditions (30, 32). (B) Linear absorption spectra of the wild-type oxidized (blue) and wild-type reduced (red) FMO complex at 77 K. Shown in gray is the laser spectrum used. (C and D) Rephasing 2D electronic spectra under oxidizing and reducing conditions at waiting time T = 40 fs. Differences in the lower-diagonal cross-peaks between experiments indicate faster, more efficient energy transfer when the complex is reduced.

Fig. 2.

Rephasing power spectra for oscillations in T integrated over regions of the 2D spectrum. (A) Reduced FMO 2D spectrum at T = 40 fs showing integrated regions. Regional power spectra for (B–D) below-diagonal regions and (E and F) diagonal regions. Oxidizing and reducing data are plotted in blue and red, respectively. The shaded regions represent the SE over the mean. The dashed vertical lines mark positive beating frequencies at 167 cm⁻¹, 335 cm⁻¹, and 550 cm⁻¹, shown as beating maps in the next figure. In general, the magnitude of the beating signals is larger in the reduced data below the diagonal, particularly at positive frequencies, which results from coherences on the excited state. Diagonal power spectra show similar beating magnitudes between redox conditions. All time traces were Fourier-transformed after T = 240 fs to focus on the long-lived coherent dynamics. Other integrated regions can be found in SI Appendix, Fig. S1.

Fig. 3.

Beating amplitude maps at (A and D) +167 cm⁻¹, (B and E) +335 cm⁻¹, and (C and F) +550 cm⁻¹ for rephasing FMO spectra under oxidizing and reducing conditions. The magnitude represents the relative beating strength for the ω_T frequency at each point on the 2D spectrum. A below-diagonal feature at the positive frequency only appears in reducing conditions. This region corresponds to downhill energy transfer in the complex, which is enhanced in reducing conditions (31, 32).

Fig. 4.

Proposed Feynman pathway explaining below-diagonal coherences observed at positive frequencies in the rephasing spectra. (A) Ground state bleach pathways cannot contribute to the positive frequency because the energy of g_v, where the subscript v denotes an excited vibrational quantum, is greater than g₀, producing a negative frequency in T. The stimulated emission pathway contains a coherence transfer during T between excited-state vibrational coherences on excitons 4 and 1. The observed beats below the diagonal are the vibrational coherences on exciton 1. Because e_1v > e₁, the waiting time frequency is positive. The enhanced energy transfer promoted by vibronic coupling in reducing conditions preserves the vibrational coherence (32). (B) Sliding window Fourier transform of the below-diagonal feature at +167 cm⁻¹ using a 1,000-fs window in T. The sliding trace shows that the coherence grows in with T, providing evidence for the coherence transfer pathway.