Quantum coherence spectroscopy reveals complex dynamics in bacterial light-harvesting complex 2 (LH2)

Abstract

Light-harvesting antenna complexes transfer energy from sunlight to photosynthetic reaction centers where charge separation drives cellular metabolism. The process through which pigments transfer excitation energy involves a complex choreography of coherent and incoherent processes mediated by the surrounding protein and solvent environment. The recent discovery of coherent dynamics in photosynthetic light-harvesting antennae has motivated many theoretical models exploring effects of interference in energy transfer phenomena. In this work, we provide experimental evidence of long-lived quantum coherence between the spectrally separated B800 and B850 rings of the light-harvesting complex 2 (LH2) of purple bacteria. Spectrally resolved maps of the detuning, dephasing, and the amplitude of electronic coupling between excitons reveal that different relaxation pathways act in concert for optimal transfer efficiency. Furthermore, maps of the phase of the signal suggest that quantum mechanical interference between different energy transfer pathways may be important even at ambient temperature. Such interference at a product state has already been shown to enhance the quantum efficiency of transfer in theoretical models of closed loop systems such as LH2.

Fig. 1.

LH2 linear absorption spectrum at room temperature. B800 and B850 bands from the light-harvesting complex of the photosynthetic bacterium Rhodobacter sphaeroides at room temperature. Continuum-generated pulse spectrum is shown in red. Dashed lines correspond to limits of detection for the grating and CCD combination used in these experiments.

Fig. 2.

Two-dimensional power spectra of LH2 at select waiting times. The acquisition time for each spectrum is 200 ms and is displayed normalized to its highest peak value for ease of visualization. The contour lines are displayed in increments of 0.5% from 7.5% to 9.5% and in increments of 5% from 10% to 100% of the signal maximum for each waiting time. Only the absolute value of the 2D spectra is shown even though the complex third-order nonlinear signal is measured owing to ambiguity in the global phase term. This term does not affect the analysis because it is uniform across the 2D spectrum. From previous transient absorption measurements, the large tail of the 800-nm diagonal peak toward the blue edge of the spectrum arises from excited-state absorption. The deviation of the peak maximum near the diagonal of the spectrum is a result of an ultrafast Stokes shift due to solvent reorganization.

Fig. 3.

Quantum-beating signal. (A) Two-dimensional spectrum at T = 1,000 fs normalized to its maximum value. The cross-peak above the diagonal is displayed on a different color scale to highlight features. (B) Each region inside the dashed box of A is fit to an exponentially decaying sinusoidal function. The single frequency value of the fit is displayed as a zero-quantum coherence (ZQC) beating map. This map matches the theoretical prediction based on the detuning between coherence and rephasing frequencies to within experimental error. (C) The signal as a function of the waiting time is shown for the (860 nm, 852 nm) voxel along with a fit to an exponentially decaying sinusoidal function. See SI Text for more information. (D) Residual signal (black and red dots and blue fit) is plotted after subtraction of an exponential decay for two points in the region of B (x marks).

Fig. 4.

Primary factors controlling energy transfer optimization in LH2. (A) Dephasing and beating maps in the upper left cross-peak of the 2D spectrum. Maps are derived from fitting each pixel in the 2D spectrum to the functional form described in the text. The dephasing map is a measure of the extent of system–bath interactions during the waiting period. The amplitude map is proportional to the strength of electronic coupling between excitons on each of the two subunits of LH2. Cuts through the dephasing time (red dashed lines) and amplitude (black dashed lines) maps showing strong anticorrelation. (B) The phase map modulates the quantum mechanical interference between different energy transfer pathways. Cut through a fixed value of the rephasing frequency at 794 nm is shown to the right.

Fig. 5.

Schematic representation of quantum phase interferometry. In LH2, we observe three states coupled together in a loop configuration. Relaxation through different pathways (red and blue) can lead to interference at the lowest energy B850 state in an isolated LH2 complex devoid of the photosynthetic reaction center (RC). The strength of the coupling as determined by the amplitude of the beating signal is represented by the thickness of the line connecting the states (blue and red line segments). The green arrows indicate the extent of system-bath interactions determined by the dephasing rates. The experimentally determined phase terms are indicated to within 0.1 radians of the values measured.