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.

Recent advances in the structural diversity of reaction centers

“…Though green sulfur bacteria typically reside in anaerobic environments, it is clear that mechanisms are present for coping with at least low levels of oxygen. Namely, they express various antioxidant proteins (Li et al 2009 ) and the FMOs contain redox-active Cys residues for energy quenching (Orf 2016 ; Higgins 2021 ). The role of F39 in energy quenching is an important addition to our understanding of how green sulfur bacteria tolerate oxygen, but the surprising conservation of structural features in the F39 region between the GsbRC and PSII suggest that the incorporation of energy quenching mechanisms has been a powerful force in RC evolution, possibly from early on.…”

Quantum Biotechnology

“…These were initially attributed to electron coherence and used as evidence that exciton transport to the photosynthetic reaction centre was accelerated by quantum interference between multiple pathways. It has since become clear that the situation is more complex, and that these coherences likely arise due to collective vibrational motions [301,302,303], which act as an "environment" that assists exciton transport [304,305]. The robustness of environment-assisted exciton transport in nature is under active investigation as a means to engineer high efficiency quantum transport [306,307], with quantum aspects predicted to improve transport at biologically relevant timescales and temperatures [308].…”

Localisation determines the optimal noise rate for quantum transport

“…For over a decade, a lot of work has exposed the mechanisms of environmental noise-assisted quantum transport (ENAQT) [8][9][10][11][12], a phenomenon describing how incoherent processes from interactions with the environment around a system can improve energy transport in quantum systems. This work was heavily motivated by the possible connection between ENAQT and the efficiency of photosynthesis [1,3,[8][9][10][13][14][15], though recent work suggests the relationship between the two may be more nuanced [16][17][18].…”