Coherence in carotenoid-to-chlorophyll energy transfer

Abstract

The subtle details of the mechanism of energy flow from carotenoids to chlorophylls in biological light-harvesting complexes are still not fully understood, especially in the ultrafast regime. Here we focus on the antenna complex peridinin-chlorophyll a-protein (PCP), known for its remarkable efficiency of excitation energy transfer from carotenoids-peridinins-to chlorophylls. PCP solutions are studied by means of 2D electronic spectroscopy in different experimental conditions. Together with a global kinetic analysis and multiscale quantum chemical calculations, these data allow us to comprehensively address the contribution of the potential pathways of energy flow in PCP. These data support dominant energy transfer from peridinin S₂ to chlorophyll Q_y state via an ultrafast coherent mechanism. The coherent superposition of the two states is functional to drive population to the final acceptor state, adding an important piece of information in the quest for connections between coherent phenomena and biological functions.

Fig. 1

PCP linear absorption spectrum. Experimental spectrum (black solid line) in sodium phosphate buffer (pH 7.5) and laser spectrum profiles (colored lines) used in the three 2DES experiments. Calculated excitonic spectrum (black dotted line) and corresponding positions of the excitonic states (gray bars). Orange and green bars show the absorption regions of Pers and Chls, respectively

Fig. 2

Results of quantum mechanical simulations. a Structure of the Per624–Chl602 pair. b Electrostatic potential on the molecular surface of Per624 due to the protein environment. c Average spectral density calculated for the Pers (red) compared with the Fourier transform of the oscillating part of the 2DES signal recorded with laser 3 (gray) (see also Supplementary Fig. 1). d Calculated two-dimensional heat map of the correlation between the zero-phonon energy of the Per exciton (x-axis) and the S₂ → Q_y EET rates (y-axis). The color bar represents the number of occurrences. Some regions of the heat map are labeled with the Per, which the exciton is localized on. The numeric labels pinpoint distinct chromophores as described in ref.

Fig. 3

Absorptive 2DES signal of PCP at 295 K. a–c Experimental and d–f simulated 2DES maps at a selected value of population time (100 fs) obtained with laser 1 (a, d), laser 2 (b, e), and laser 3 (c, f), respectively. More details of experimental and simulated data are reported in Supplementary Fig. 11–13. Maps are normalized to 1 at their maximum. The dots labeled from A to F in a pinpoint relevant positions as commented in the main text for all the laser bandwidths. g 2DES maps recorded with laser 3 at different population times

Fig. 4

Experimental and simulated time traces extracted at relevant coordinates in the real absorptive 2DES maps. See points A and E in Fig. 3b. Red, yellow, and blue lines point out measures performed with laser 1, 2, and 3, respectively. a Experimental data (thin lines) and results of the global kinetic analysis (thick lines) at cross-peak coordinates E, (17 500, 14 850) cm⁻¹. Laser 2 and 3 traces are shifted by 0.2 and 0.4, respectively, to help visualization. Feynman diagrams describing the EET pathways giving rise to signal in E are also shown. b Experimental signal (thin lines) and fitting traces (thick lines) integrated over the diagonal Q_y signal at coordinates A (14 850, 14 850) cm⁻¹. Feynman diagram describing the rising signal in A. Traces recorded with laser 2 and 3 are shifted by 200 and 400 units, respectively. c Simulated real absorptive signal at cross-peak E

Fig. 5

Kinetic analysis. a Kinetic scheme of excitation energy transfer pathways in PCP. b Time evolution of populations according to the results of the fitting based on the kinetic model in a. c Lognormal distribution of S₂ → Q_y transfer rates. Shaded area suggests the time domain of coherent EET

Fig. 6

Analysis of the beating behavior of the S₂/Q_y cross-peak. a The coordinates at which the analysis has been performed are pinpointed as colored dots in a 2DES map. b Time traces at the corresponding coordinates. Note the break in the time axis at 100 fs. c Fourier transform (FT) of the traces in b computed in the time windows (0:1000) fs (left) and (75:1000) fs (right), confirming that the broad component centered at about 1900 cm⁻¹ is a quickly dephasing signal and not just a FT artifact. d Time-frequency transform of the trace at (17 800, 14 850) cm⁻¹