Impact of Fluctuations in the Peridinin-Chlorophyll a-Protein on the Energy Transfer: Insights from Classical and QM/MM Molecular Dynamics Simulations

Abstract

The peridinin-chlorophyll a-protein is a light-harvesting complex found in dinoflagellates, which has an unusually high fraction of carotenoids. The carotenoids are directly involved in the energy transfer to chlorophyll with high efficiency. The detailed mechanism of energy transfer and the roles of the protein in the process remain debated in the literature, in part because most calculations have focused on a limited number of chromophore structures. Here we investigate the magnitude of the fluctuations of the site energies of individual and coupled chromophores, as the results are essential to the understanding of experimental spectra and the energy transfer mechanism. To this end, we sampled conformations of the PCP complex by means of classical and quantum mechanical/molecular mechanical (QM/MM) molecular dynamics simulations. Subsequently we performed (supermolecular) excitation energy calculations on a statistically significant number of snapshots using TD-LC-DFT/CAM-B3LYP and the semiempirical time-dependent long-range corrected density functional tight binding (TD-LC-DFTB2) as the QM method. We observed that the magnitude of the site energy fluctuations is large compared to the differences of the site energies between the chromophores, and this also holds for the coupled chromophores. We also investigated the composition of the coupled states, the effect of coupling on the absorption spectra, as well as transition dipole moment orientations and the possibility of delocalized states with Chl a. Our study thus complements previous computational studies relying on a single structure and establishes the most prominent features of the coupled chromophores that are essential to the robustness of the energy transfer process.

Figure 1:

Structure of the PCP complex. Top left: full trimer (crystal structure: 1PPR) with chlorophylls in green, glycolipids in black and peridinins in orange. Top right: one monomer (based on crystal structure 3IIS) with chlorophylls in green, glycolipids in black, and different peridinins in different colours: Per611-yellow, Per612-red, Per613-orange, Per614-pink. Bottom: the chemical structure of peridinin. Special features of this carotenoid are highlighted by colour: epoxid-red, lactone-green, allene-blue.

Figure 2:

Root mean square deviation (RMSD) of peridinin geometries of domain a along the 100 ns of classical MD simulation trajectory with respect to the crystal structure. Note the large change in Per-613 due to a dihedral rotation (Fig. S14); see discussion in the text.

Figure 3:

Site energies and oscillator strengths computed with TD-LC-DFTB2/OB2 of 1,000 snapshots equally spaced along the last 20 ns of the classical MD trajectory (domain a). Running averages over 100 data points are shown as well.

Figure 4:

Difference in surrounding of conjugated chain of per614 in domain a and b in the evaluated trajectory piece. Top: In domain a the amino moiety of Asn 89 interacts with a water molecule and the oxygen of the side chain points towards the peridinin chain. Bottom: In domain b the Asn 89 side chain is rotated and the amino moiety forms a hydrogen bond with the tryptophan backbone.

Figure 5:

Top: Contributions of individual peridinins to the coupled state with the highest oscillator strength (almost always state 4) according to the first four NTO coefficients which were assigned to the peridinins through orbital plots. One calculation is left out because it predicted five low-lying bright states. Bottom: NTOs of the bright state in one snapshot (calc. 12) which has almost equal contributions of the four peridinins. The first row contains the hole orbitals, and the second row the particle orbitals.

Figure 6:

Left: coupled site energies (supermolecular excitation energies) computed with TD-CAM-B3LYP considering the environment via point charges. The symbols indicate the pigment with the main contribution to the respective excitation, while the color helps to distinguish the energetical order. Right: oscillator strengths of individual and coupled peridinins. The oscillator strengths of the supermolecular excitations also carry the symbol of the peridinin with the largest contribution and are coloured according to the energetic order of the (bright) coupled states. The results of four calculations are left out because the assignment of the peridinins to the excitation energies was nondistinctive.

Figure 7:

Histograms of excitation energies of all eight pigments in the PCP monomer, computed with TD-CAM-B3LYP (20 snapshots × 2 domains × 4 pigments = 160 values) under different conditions (with (pc) and without (vac) point charges, single (uncpl) and supermolecule (cpl) calculations). The bright 1B_u state of the single peridinins and the four brightest low-lying states of the coupled peridinins were considered. On the right plot, the counts in each bin were not only normalized but subsequently scaled by the average of the oscillator strengths belonging to the excitation energies in that bin.

Figure 8:

A graphic summary of the key features of the energy transfer mechanism in PCP based on the computations conducted in this work. (Left) The peridinins are coupled, leading to bright excitonic states of different degrees of mixing. The highest energy excitonic state features the largest oscillator strength and also the highest degree of mixing, and lower energy states are more localized in nature; the colors indicate the average contributions of individual peridinins. (Right) The coupling of peridinins leads to the reorientation of transition dipoles, so that the highest energy state is better aligned, on average, with the transition dipole of the Q_x state of Chl a, while the lower energy excitonic states of the peridinins feature similar angles with both Q_x and Q_y states of Chl a. Therefore, the calculations suggest that the exciton is initially delocalized among the peridinins and then becomes increasingly localized in nature and ultimately transfers energy to both Q_x and Q_y of Chl a.