Protein Effects on the Excitation Energies and Exciton Dynamics of the CP24 Antenna Complex

Abstract

In this study, the site energy fluctuations, energy transfer dynamics, and some spectroscopic properties of the minor light-harvesting complex CP24 in a membrane environment were determined. For this purpose, a 3 μs-long classical molecular dynamics simulation was performed for the CP24 complex. Furthermore, using the density functional tight binding/molecular mechanics molecular dynamics (DFTB/MM MD) approach, we performed excited state calculations for the chlorophyll a and chlorophyll b molecules in the complex starting from five different positions of the MD trajectory. During the extended simulations, we observed variations in the site energies of the different sets as a result of the fluctuating protein environment. In particular, a water coordination to Chl-b 608 occurred only after about 1 μs in the simulations, demonstrating dynamic changes in the environment of this pigment. From the classical and the DFTB/MM MD simulations, spectral densities and the (time-dependent) Hamiltonian of the complex were determined. Based on these results, three independent strongly coupled chlorophyll clusters were revealed within the complex. In addition, absorption and fluorescence spectra were determined together with the exciton relaxation dynamics, which reasonably well agrees with experimental time scales.

Figure 1

Left panel: a cartoon representation of the cryo-EM structure of the CP24 complex (PDB ID: 5XNL). The structure contains Chl-a, Chl-b and carotenoid molecules represented as sticks in different colors: Chl-a in blue, Chl-b in green, lutein in silver, violaxanthin in orange, and β-carotene in pink. Right panel: Side view of the arrangement of the Chl-a and Chl-b pigments within the complex. Only the porphyrin rings of the chlorophyll molecules without the phytyl tails are visualized, each labeled according to the nomenclature used in the Protein Data Bank (PDB).

Figure 2

Root-mean-square fluctuations (RMSFs) of the C-alpha atoms belonging to the CP24 complex during the 3 μs-long classical MD trajectory. The loop regions are highlighted by an orange background color.

Figure 3

Average site energies of the 11 chlorophyll pigments within CP24 derived based on five distinct sets of 1 ns-long QM/MM MD trajectories (see text). The standard deviations are represented by the error bars, which illustrate the fluctuations in the site energies.

Figure 4

Comparison of average site energies of all chlorophyll molecules within the CP24 complex obtained from the 1 ns-long QM/MM MD trajectories belonging to set 1 (left) and set 3 (right). The error bars indicate the standard deviations of the energy fluctuations. The excitation energy calculations along the pieces of the trajectory have been executed including and excluding (“no env”) the point charges in the MM environments.

Figure 5

Dynamic coordination of water molecules within 2.5 Å nm of Mg in Chl-b 608 over the 3 μs-long MD simulation.

Figure 6

Dynamic coordination of water molecules within 2.5 Å of Mg in chlorophyll molecule 608 from 5 initial configurations. The water molecules are coordinated to the Mg atom in sets 3, 4 and 5.

Figure 7

Average site energies of the pigments in the CP24 complex along the 1 ns-long trajectory using TD-LC-DFTB. The present findings (average of sets 3, 4 and 5) are compared to the site energies of the CP29 and LHCII complexes as determined by Müh et al. based on the crystal structure. The LHCII site energies are shifted by 0.203 eV and the CP29 energies by 0.207 eV for better comparison.

Figure 8

Comparison of the spectral densities of the CP24 complex averaged over all pigments in the system. The result is based on 60 ps-long QM/MM MD trajectories from sets 1 and 3. The spectral density for the CP29 complex has been obtained in a similar manner. Also shown is the experimental spectral density of the LHCII complex.

Figure 9

Based on the excitonic coupling values, the chlorophyll molecules in the CP24 complex are arranged in different clusters, as indicated by the different colors. Left: side view, right: top view.

Figure 10

Absorption spectra of the CP24 complex based on the FCE and Redfield methods compared to the experimental spectrum at room temperature. The FCE and the Redfield data have been shifted by 0.10 and 0.16 eV, respectively, toward lower energies to match the position of the main experimental peak.

Figure 11

Fluorescence spectra of the CP24 complex based on the Redfield method compared to the experimental results. The Redfield data has been shifted by 0.16 eV toward lower energies to match the experimental peak position.

Figure 12

Exciton dynamics in the CP24 complex based on TD-LC-DFTB. While in panel (a) Chl-a 603 is initially excited, the initial excitations is on Chl-a 604 in panel (b) and on Chl-b 608 in panel (c).