Direct evidence of quantum transport in photosynthetic light-harvesting complexes

Abstract

The photosynthetic light-harvesting apparatus moves energy from absorbed photons to the reaction center with remarkable quantum efficiency. Recently, long-lived quantum coherence has been proposed to influence efficiency and robustness of photosynthetic energy transfer in light-harvesting antennae. The quantum aspect of these dynamics has generated great interest both because of the possibility for efficient long-range energy transfer and because biology is typically considered to operate entirely in the classical regime. Yet, experiments to date show only that coherence persists long enough that it can influence dynamics, but they have not directly shown that coherence does influence energy transfer. Here, we provide experimental evidence that interaction between the bacteriochlorophyll chromophores and the protein environment surrounding them not only prolongs quantum coherence, but also spawns reversible, oscillatory energy transfer among excited states. Using two-dimensional electronic spectroscopy, we observe oscillatory excited-state populations demonstrating that quantum transport of energy occurs in biological systems. The observed population oscillation suggests that these light-harvesting antennae trade energy reversibly between the protein and the chromophores. Resolving design principles evident in this biological antenna could provide inspiration for new solar energy applications.

Fig. 1.

The Redfield relaxation superoperator contains three types of transfer elements: transfer between populations (blue), transfer between coherences (green), and transfer between a population and a coherence (red). These transfer mechanisms are depicted schematically both in the FMO photosynthetic antenna complex and in the density matrix. Quantum transport (red) occurs when populations and coherences directly couple. Each transfer scheme implies a different type of interaction with the protein environment, with the most active contribution occurring in the quantum transport regime.

Fig. 2.

An overlay of quantum coherence beating (green) and population oscillation (red) highlights the 90° phase shift in the experimental signals extracted from rephasing data. This observed phase shift results from a coupling between the oscillating coherence signal to the time-derivative of population dynamics. The experimental data are shown in solid circles connected by dashed lines, and the fits are shown in solid lines. A representative 2D spectrum from a rephasing pathway at T = 1,260 fs is shown in the Inset; the green and red circles highlight the spectral position from which the signals are extracted. The fit of the population oscillation signal is obtained by adjusting only the phase and amplitudes of the fit of the coherence signal. Although the model successfully captures the frequency and position of the extrema, the population signal also couples to other coherences giving rise to fluctuations not captured by this model.

Fig. 3.

Two-dimensional data filtered in the waiting time, T, domain using a z-transform to select long-lived beating signals (dephasing rate, Γ, less than 30 cm^-1) with a beat frequency, ω_T, between 155 and 163 cm^-1 corresponding to the energy difference between excitons 1 and 2. For each point in the spectrum, the saturation (whiteness) is determined by whether the data shows a long-lived beating signal of the appropriate frequency, whereas the hue is determined by the amplitude (A) or phase (B) of the beating signal. The colored regions show that the beating signal appears only on the cross-peak and associated diagonal peak, suggesting electronic quantum coherence as the origin of the signal. In contrast, an oscillatory signal due to vibrational coherence or power fluctuations would appear throughout the spectrum. The 90° phase difference between the coherence (off-diagonal) and population (diagonal) signals is a signature of quantum transport. Contour lines from the T = 1,260 fs spectra from Fig. 2 are included in light gray for reference.