Femtosecond Heterodyne Transient Grating Studies of Nonradiative Deactivation of the S₂ (1¹B_u⁺) State of Peridinin: Detection and Spectroscopic Assignment of an Intermediate in the Decay Pathway

Abstract

Femtosecond heterodyne transient grating spectroscopy was employed to investigate the nonradiative decay pathway from the S2 (1(1)Bu(+)) state to the S1 (2(1)Ag(-)) state of peridinin in methanol solution. Just as previously observed by this laboratory for β-carotene in benzonitrile, the real (absorption) and imaginary (dispersion) components of the transient grating signal obtained with Fourier transform spectral interferometry from peridinin exhibit ultrafast responses indicating that S2 state decays in 12 fs to produce an intermediate state, Sx. The excited state absorption spectrum from the Sx state of peridinin, however, is found to be markedly blue-shifted from that of β-carotene because it makes a substantial contribution to the signal observed with 40 fs, 520 nm pulses. The results of a global target analysis and numerical simulations using nonlinear response functions and the multimode Brownian oscillator model support the assignment of Sx to a displaced conformation of the S2 state rather than to a vibrationally excited (or hot) S1 state. The Sx state in peridinin is assigned to a structure with a distorted conjugated polyene backbone moving past an activation-energy barrier between planar and twisted structures on the S2 potential surface. The lengthened lifetime of the Sx state of peridinin in methanol, 900 ± 100 fs, much longer than that typically observed for carotenoids lacking carbonyl substituents, ∼150 fs, can be attributed to the slowing of torsional motions by solvent friction. In peridinin, the system-bath coupling is significantly enhanced over that in β-carotene solution most likely due to the intrinsic intramolecular charge transfer character it derives from the electron withdrawing nature of the carbonyl substituent. An important additional implication is that the Sx state, and the distorted structures reached subsequently along the torsional gradient on the S2 potential surface, may serve as the principal excitation energy transfer donors to chlorophyll a in the peridinin-chlorophyll a protein from dinoflagellates.

Torsional Dynamics and Intramolecular Charge Transfer in the S2 (11Bu+) Excited State of Peridinin: A Mechanism for Enhanced Mid-Visible Light Harvesting

“…The viscosity dependence reported here for the lifetime of the S x state, however, establishes for the first time that large-amplitude torsional motions promote nonradiative decay from S x to S 1 . As is also observed for the decay of excited states in triphenylmethane (TPM) dyes and in cyanines, the lifetime of the S x state follows a power law function with respect to the solvent viscosity (Figure a), which indicates that solvent friction retards progress along torsional coordinates toward a position-sensitive sink (or seam ,, ) leading to the S 1 state. But a better correlation of the lifetime of S x is obtained with respect to the average polar solvation time (Figure b), which suggests that the friction that slows the decay from S x to S 1 includes a solvent reorganization in response to the net transfer of charge that accompanies the twisting and pyramidalization of a CC bond. − A comparable lifetime dependence was observed in the dye LDS–821, which exhibits a twisted intramolecular charge-transfer (TICT) excited state …”

“…Instead, as proposed previously, ,, the S x state is best assigned to a twisted form of the S 2 state. The time evolution of the high-frequency, CC bond stretching bands recently observed using transient IR and stimulated Raman spectroscopy by Di Donato et al supports the previous conclusion from pump–probe and pump–dump–probe spectroscopy by Zigmantas et al and Papagiannakis et al, respectively, that distortions of the conjugated polyene backbone of peridinin occur after optical preparation of the S 2 state.…”

Uncovering dark multichromophoric states in Peridinin–Chlorophyll–Protein

“…Nonetheless, this framework ignores the unique chemical nature of the peridinin Car-containing an allene tail and a lactone ring-that may support intramolecular-charge-transfer (ICT) character and even a separate ICT state [20]. Yet much like the claims of spectral evidence for dark intermediate states, the nature of ICT in peridinin remains controversially assigned, as evidenced by twenty-first-century experimental [21][22][23] and computational [24][25][26][27] investigations. On one hand, red-shifted emission with diminished lifetime in the face of polar solvent [20] and a distinct low-lying electronic excited state with ICT character [24] have been reported; on the other hand, conformational bright-state local minima [21,22] and bond-vibration-driven interplay between the lowest-lying bright-and dark-state properties [25] have been proposed as explanations for peridinin's anomalous photophysics.…”

“…Yet much like the claims of spectral evidence for dark intermediate states, the nature of ICT in peridinin remains controversially assigned, as evidenced by twenty-first-century experimental [21][22][23] and computational [24][25][26][27] investigations. On one hand, red-shifted emission with diminished lifetime in the face of polar solvent [20] and a distinct low-lying electronic excited state with ICT character [24] have been reported; on the other hand, conformational bright-state local minima [21,22] and bond-vibration-driven interplay between the lowest-lying bright-and dark-state properties [25] have been proposed as explanations for peridinin's anomalous photophysics. Whether ICT character exists as its own independent electronic excited state, and whether it impacts S 2 /S 1 state properties, may have important implications in energy transfer.…”

Solvent-Dependent Characterization of Fucoxanthin through 2D Electronic Spectroscopy Reveals New Details on the Intramolecular Charge-Transfer State Dynamics

“…This picture seems to be also supported by the work of Ghosh et al, who identified a <20 fs nonradiative decay of the S 2 of peridinin to an S x state with a strong ICT character, assigned to a distorted configuration. 47 , 57 …”