Peridinin Torsional Distortion and Bond-Length Alternation Introduce Intramolecular Charge-Transfer and Correlated Triplet Pair Intermediate Excited States

Abstract

The nature of intramolecular charge transfer (ICT) and the mechanism of intramolecular singlet fission (SF) in peridinin remain open research questions. Obtaining an understanding of the population evolution from the bright state to dark state following a photoinduced electronic transition is critical. Unambiguously describing this evolution in peridinin, and light-harvesting carotenoids in general, has proven elusive experimentally and computationally. To offer a balanced description of the bright- and dark-state electronic structures, we here apply ab initio multireference perturbation theory quantum chemistry-the density matrix renormalization group self-consistent field and complete-active-space self-consistent field with second-order N-electron valence perturbation theory. At traditional bright- (S) and dark-state (S) optimized geometries, we find that an additional correlated triplet pair state and ICT state are derived from the canonical polyene B (S) and 3A (S) dark singlet excited states, respectively. Whereas the S state's physical properties are insensitive to peridinin's allene-tail donor and lactone ring acceptor functionalization, the S state exhibits a markedly enhanced oscillator strength and highest occupied molecular orbital-lowest unoccupied molecular orbital transition density. These changes suggest that the ICT character stems from mixing between the bright S and putatively dark S.

Uncovering dark multichromophoric states in Peridinin–Chlorophyll–Protein

“…Given that the S 1 state is below the S 2 state by only 0.12 eV in the crystal-structure geometry of peridinin 611N, it would seem that these two states would be able to couple directly through off-diagonal elements of the nuclear kinetic energy operator-vibronic coupling-without a bridging intermediate state. S 1 and S 2 appear traceable to the dark and bright states of polyenes based on their predominant wave function configurations as we previously noted [45].…”

“…The counter-intuitive nuclear reorganization in S 2 from the crystal structure-a highly distorted peridinin conformationinvolves C=C contraction rather than elongation as we have reported previously for polyenes [47] and for peridinin [45] from an S 0 equilibrium geometry. Owing to intrinsic uncertainty in the protein crystal structure, it is unclear as to whether the geometric distortions in the 611N crystal-structure geometry are consequences of biological orientation or artefacts of extracting nuclear coordinates from a crystal structure.…”

“…These include sub-200-fs singlet fission observed previously in carotenoid aggregates [44] and sub-200-fs ground-state bleaching of Chl-a stemming from hole generation following Car optical excitation in ultrafast laser spectroscopy [3,27,28]. We also present quantum chemical evidence for direct peridinin S 2 -S 1 internal conversion in the single-molecule picture without the involvement of intermediate states-ICT or otherwise-with S 1 falling below the photoexcited-state energy following nuclear reorganization as we, and others, have previously found [25,45,46]. The lowest-lying Car bright and dark states are shown to be quasidegenerate prior to S 1 population.…”

“…Our results stem from the application of multireference state-averaged complete-active-space self-consistent field royalsocietypublishing.org/journal/rsif J. R. Soc. Interface 17: 20190736 (CASSCF) and its approximate density-matrix-renormalization-group (DMRGSCF) form paired with second-order N-electron valence-state perturbation theory (NEVPT2)-an approach we have applied previously [45,47,48]-to capture the different electron-correlation types defining bright and dark states. Our optimal results from the best variational wave functions, tabulated in table 1 and graphically displayed in figure 1 for different active spaces, suggest that the S 1 and S 2 states are quasidegenerate for 611N in its crystal structure.…”

“…We have detailed our application of CASSCF/DMRGSCF and NEVPT2 in prior publications [45,47,48]. Briefly, we considered the variational quality of the wave functions computed across different active spaces by comparing variational CAS/DMRGSCF excitation energies with those after applying NEVPT2.…”