Photosynthesis tunes quantum-mechanical mixing of electronic and vibrational states to steer exciton energy transfer

Abstract

Photosynthetic species evolved to protect their light-harvesting apparatus from photoxidative damage driven by intracellular redox conditions or environmental conditions. The Fenna-Matthews-Olson (FMO) pigment-protein complex from green sulfur bacteria exhibits redox-dependent quenching behavior partially due to two internal cysteine residues. Here, we show evidence that a photosynthetic complex exploits the quantum mechanics of vibronic mixing to activate an oxidative photoprotective mechanism. We use two-dimensional electronic spectroscopy (2DES) to capture energy transfer dynamics in wild-type and cysteine-deficient FMO mutant proteins under both reducing and oxidizing conditions. Under reducing conditions, we find equal energy transfer through the exciton 4-1 and 4-2-1 pathways because the exciton 4-1 energy gap is vibronically coupled with a bacteriochlorophyll-a vibrational mode. Under oxidizing conditions, however, the resonance of the exciton 4-1 energy gap is detuned from the vibrational mode, causing excitons to preferentially steer through the indirect 4-2-1 pathway to increase the likelihood of exciton quenching. We use a Redfield model to show that the complex achieves this effect by tuning the site III energy via the redox state of its internal cysteine residues. This result shows how pigment-protein complexes exploit the quantum mechanics of vibronic coupling to steer energy transfer.

Keywords: excitonic energy transfer; photosynthesis; quantum effects in biology; ultrafast spectroscopy; vibronic coupling.

Fig. 1.

(Left) Numbered sites and sidechains of cysteines C353 and C49 in the FMO pigment–protein complex (PDB ID code: 3ENI) (20). (Right) Site densities for excitons 4, 2, and 1 in reducing conditions with the energy transfer branching ratios for the WT oxidized and reduced protein. The saturation of pigments in each exciton denotes the relative contribution number to the exciton. The C353 residue is located near excitons 4 and 2, which have most electron density along one side of the complex, and other redox-active residues such as the Trp/Tyr chain. C353 and C49 surround site III, which contains the majority of exciton 1 density. Excitons 2 and 4 are generally delocalized over sites IV, V, and VII.

Fig. 2.

Absorptive 2D spectra of the eight FMO samples taken at 77 K at waiting time T = 1 ps under reducing (A–D, Top Row) and oxidizing (E–H, Bottom Row) conditions. In 2DES, the excitation energy of a system is correlated with the detection energy, and the waiting time T indicates the delay time between the pump and probe pulses. Spectra were normalized to the peak amplitude at time T = 0. The three peaks of the diagonal features in each spectrum represent excitons 4, 2, and 1. The growth of cross-peaks below the diagonal indicates downhill EET on the timescale of hundreds of femtoseconds.

Fig. 3.

Calculated Redfield energy transfer rates of the FMO Hamiltonian upon changing the site energies and degree of system–bath coupling (Huang–Rhys factors, S) for pigments III (A and B) and IV (C and D). The center points (S/S₀ = 1; site energy change $\mathrm{\Delta }\nu$ = 0 cm⁻¹; plotted as red circle) represent the WT FMO in reducing conditions. The blue circles represent WT FMO in oxidizing conditions. (A) Overlap of the distribution of exciton 4–1 energy gaps in FMO with the spectral density for site III, representing relative vibronic coupling with an intramolecular vibration. Increased overlap with the spectral density indicates that the bath can more readily couple the two excitons, which increases the EET rate. (B) Change in the τ₄₁ time constant as site III energy and Huang–Rhys factor is changed. (C and D) Change in the τ₂₁ and τ₄₂ time constants as site IV is changed. The arrows represent how mutation changes each FMO sample. The “o” and “r “prefixes represent the oxidized and reduced parameters, respectively. For the reduced FMO samples, there is no change in the C49A parameters, and the C353A changes are the same as the double-mutant (DM) changes. In every case, the DM is a sum of the two single-mutant vectors. The calculated changes in all parameters and the associated energy transfer constants are shown in Table 1 under “Redfield theory.” The same plots but with arrows plotted as oxidation vectors are shown in SI Appendix.