Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’

Abstract

Plants possess an essential ability to rapidly down-regulate light-harvesting in response to high light. This photoprotective process involves the formation of energy-quenching interactions between the chlorophyll and carotenoid pigments within the antenna of Photosystem II (PSII). The nature of these interactions is currently debated, with, among others, 'incoherent' or 'coherent' quenching models (or a combination of the two) suggested by a range of time-resolved spectroscopic measurements. In 'incoherent quenching', energy is transferred from a chlorophyll to a carotenoid and is dissipated due to the intrinsically short excitation lifetime of the latter. 'Coherent quenching' would arise from the quantum mechanical mixing of chlorophyll and carotenoid excited state properties, leading to a reduction in chlorophyll excitation lifetime. The key parameters are the energy gap, Δ = Car − Chl , and the resonance coupling, J, between the two excited states. Coherent quenching will be the dominant process when −J < Δ < J, i.e., when the two molecules are resonant, while the quenching will be largely incoherent when Chl > ( Car + J). One would expect quenching to be energetically unfavorable for Chl < ( Car − J). The actual dynamics of quenching lie somewhere between these limiting regimes and have non-trivial dependencies of both J and Δ . Using the Hierarchical Equation of Motion (HEOM) formalism we present a detailed theoretical examination of these excitation dynamics and their dependence on slow variations in J and Δ . We first consider an isolated chlorophyllcarotenoid dimer before embedding it within a PSII antenna sub-unit (LHCII). We show that neither energy transfer, nor the mixing of excited state lifetimes represent unique or necessary pathways for quenching and in fact discussing them as distinct quenching mechanisms is misleading. However, we do show that quenching cannot be switched 'on' and 'off' by fine tuning of Δ around the resonance point, Δ = 0. Due to the large reorganization energy of the carotenoid excited state, we find that the presence (or absence) of coherent interactions have almost no impact of the dynamics of quenching. Counterintuitively significant quenching is present even when the carotenoid excited state lies above that of the chlorophyll. We also show that, above a rather small threshold value of J > 10 cm −1 quenching becomes less and less sensitive to J (since in the window −J < Δ < J the overall lifetime is independent of it). The requirement for quenching appear to be only that J > 0. Although the coherent/incoherent character of the quenching can vary, the overall kinetics are likely robust with respect to fluctuations in J and Δ . This may be the basis for previous observations of NPQ with both coherent and incoherent features. energy gap, Δ , and resonance coupling, J. The solid lines are contours indicating points where the lifetime of the state is the same. e The same for the short-lived Car-like state ( |ex2 >). f, g are a clearer representation of the data in (d, e) for re...

Trivial Excitation Energy Transfer to Carotenoids is an Unlikely Mechanism for Non-Photochemical Quenching in LHCII

“…Excitonic mixing among the Chls naturally mixes these couplings, the strongest (|J 0 i,Lut | ≈ 7cm −1 ) being between Lut1 and |T E − ⟩ and |T E + ⟩. These small couplings fully justify [52] our mixed kinetic model in which the Chl excitonic and Lut1 vibronic subsystems can exchange energy incoherently.…”

“…We do not calculate the Chl excitation (site) energies but simply take the average values reported in [35]. The reason for this is partly to spare computational expense and partly because these fluctuations have almost no effect on quenching [52].…”

“…An earlier NPQ model proposed that quenching was induced by bringing the Chl Q y band and S 1 into resonance [25], which would require either ε 00 S 1 or ε 10 S 1 ≈ 15, 000cm −1 . Balevičius Jr. and Duffy recently provided a very general physical argument as to why fine tuning of this energy gap cannot modulate quenching [52] and showed that significant quenching is possible for large energy gaps, even if the quenching state lies above the donor state. S 1 has to be quite far above the Q y band to abolish quenching, as was recently proposed by Lapillo et al [45].…”

Ultrafast energy transfer between lipid-linked chromophores and plant light-harvesting complex II

“…These rates also depend on the normalised spectral overlap between donor and acceptor transitions, which was calculated using an experimentally-derived TR fluorescence spectrum 60 while the Chl Q y /Q x transitions were assigned Gaussian lineshapes and computed using a standard model of the system-bath interaction. 77 Strictly, the acceptor states in LHCII will be a mixture of single-molecule and excitonic states; however, since excitonic interactions in LHCII do not appear to produce significant peak shifts or redistribution of oscillator strengths, 77 they can be neglected without qualitatively altering the calculated rates. The total rate was then defined as the sum of all rates associated with a single TR.…”

A Protein Environment-Modulated Energy Dissipation Channel in LHCII Antenna Complex

“…The appearance of the 515 nm is instantaneous with our ∼100 fs time resolution, which, if it really is a reflection of Chl-Car energy transfer, would require very strong Chl-Car couplings. Interestingly, it was recently argued that strong couplings and fast transfer do not result overall in particularly strong quenching ( Balevičius and Duffy, 2020 ). This is due to an entropic effect in which the strongly coupled Chl-Lut pair gradually receives energy from a much larger Chl pool.…”