A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis

Abstract

Under excess illumination, plant photosystem II dissipates excess energy through the quenching of chlorophyll fluorescence, a process known as nonphotochemical quenching. Activation of nonphotochemical quenching has been linked to the conversion of a carotenoid with a conjugation length of nine double bonds (violaxanthin) into an 11-double-bond carotenoid (zeaxanthin). It has been suggested that the increase in the conjugation length turns the carotenoid from a nonquencher into a quencher of chlorophyll singlet excited states, but unequivocal evidence is lacking. Here, we present a transient absorption spectroscopic study on a model system made up of a zinc phthalocyanine (Pc) molecule covalently linked to carotenoids with 9, 10, or 11 conjugated carbon-carbon double bonds. We show that a carotenoid can act as an acceptor of Pc excitation energy, thereby shortening its singlet excited-state lifetime. The conjugation length of the carotenoid is critical to the quenching process. Remarkably, the addition of only one double bond can turn the carotenoid from a nonquencher into a very strong quencher. By studying the solvent polarity dependence of the quenching using target analysis of the time-resolved data, we show that the quenching proceeds through energy transfer from the excited Pc to the optically forbidden S(1) state of the carotenoid, coupled to an intramolecular charge-transfer state. The mechanism for excess energy dissipation in photosystem II is discussed in view of the insights obtained on this simple model system.

Fig. 1.

Molecular structures and absorption spectra of the compounds. (Upper) Molecular structures of the dyads. A zinc-Pc is covalently linked to a carotenoid with 9 conjugated carbon–carbon double bonds (dyad 1), 10 carbon–carbon double bonds (dyad 2), and 11 carbon–carbon double bonds (dyad 3). Model Pc 4 bears a hexanoyl group instead of a polyene. Model carotenoid 2′ has a terminal ester instead of a Pc. (Lower) Absorption spectrum in THF for dyad 1 (dashed line), dyad 2 (dashed-dotted line), dyad 3 (dotted line), and model Pc 4 (solid line).

Fig. 2.

Kinetic traces and global analysis of the time-resolved data. (A) Kinetic traces with excitation and detection at 680 nm for model Pc 4 (red line), dyad 1 (blue line), dyad 2 (green line), and dyad 3 (magenta line) in THF, along with the result of the global analysis fit (thin solid line). (B) EADS that follow from a global analysis of data for dyad 1. (Inset) An expanded view of the EADS in the spectral region from 475 to 620 nm. (C) The same as for B for dyad 2. (D) The same as for B for dyad 3. The difference spectra corresponding to the vibrationally relaxed, fully solvated Q_y state for model Pc 4, as determined from a global analysis, are also shown in B–D as black dashed lines.

Fig. 3.

Kinetic traces with excitation and detection at 680 nm for dyad 1 (solid line), dyad 2 (dotted line), and dyad 3 (dashed line) in acetone. The gray lines denote the result of a global analysis.

Fig. 4.

Target analysis of the time-resolved data. (Upper) Kinetic model used in target analysis of time-resolved data on dyads 2 and 3. (Lower) SADS from the target analysis for dyad 3 in THF. See text for details.

Fig. 5.

Schematic representation of the proposed quenching process: the energy from the Q_y state of Pc is transferred to the carotenoid ICT state, which then equilibrates with the carotenoid S₁ state before relaxation to the ground state by internal conversion. An increase in solvent polarity leads to a lowering of the ICT energy (gray to black lines).