Carotenoid-Chlorophyll Interactions in a Photosynthetic Antenna Protein: A Supramolecular QM/MM Approach

Abstract

Multichromophoric interactions control the initial events of energy capture and transfer in the light harvesting peridinin-chlorophyll a protein (PCP) from marine algae dinoflagellates. Due to the van der Waals association of the carotenoid peridinin (Per) with chlorophyll a in a unique 4:1 stoichiometric ratio, supramolecular quantum mechanical/molecular mechanical (QM/MM) calculations are essential to accurately describe structure, spectroscopy, and electronic coupling. We show that, by enabling inter-chromophore electronic coupling, substantial effects arise in the nature of the transition dipole moment and the absorption spectrum. We further hypothesize that inter-protein domain Per-Per interactions are not negligible, and are needed to explain the experimental reconstruction features of the spectrum in wild-type PCP.

Keywords: PCP; chlorophyll a; light harvesting; peridinin; supramolecular QM/MM.

Figure 1

(a) Partial view of the cofactor cluster inside a single domain of the reconstituted, recombinant peridinin-chlorophyll a protein (RFPCP) complex. Highlighted in green is the supramolecular assembly consisting of four bound peridinin (Per) molecules and one chlorophyll a (Chl a) encapsulated by the van der Waals surface of the protein. (b) Absorption spectrum of the peridinin-chlorophyll a protein (PCP) complex (ref. [4]) and chemical structure of Per. (c) Full view of the RFPCP C₂-symmetric homodimer.

Figure 2

Visualization of the S₀ → S₂ TDMs for (top panel) uncoupled and (bottom panel) coupled Pers in a functional domain of PCP. The coupled states are assigned to the Per that carries at least 50% of the excitation, and the associated TDM vector is colored to match the given Per. The black vectors point in the directions of the Qy and Qx TDMs of the uncoupled Chl a, which are shown in each part of the figure to aid a comparison of the angle between the Per and Chl a TDMs. All TDMs were calculated in the presence of the aqueously solvated PCP complex.

Figure 3

Simulated absorption spectra for the uncoupled (dark blue) and coupled (light blue) four Pers of a cofactor cluster in the solvated PCP complex. Gaussians with a full width at half maximum of 8 nm were fit to the calculated excitation wavelengths.

Figure 4

Simulated spectra for Per tetramers at the time dependent density functional theory (TD-DFT) (black) and configuration interaction with singles (CIS) (orange) levels of theory, and an octamer of Pers treated with CIS (purple), within the aqueously solvated PCP complex. All CIS wavelengths were systematically shifted by 0.671 eV to align the longest wavelength absorption with the corresponding TD-DFT band in order to aid a comparison. Gaussians with a full width at half maximum of 4 nm were fit to the calculated excitation wavelengths.