Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor

Abstract

Based on the structural analysis of photosystem II of Thermosynechococcus elongatus, a detailed calculation of optical properties of reaction-center (D1-D2) complexes is presented applying a theory developed previously. The calculations of absorption, linear dichroism, circular dichroism, fluorescence spectra, all at 6 K, and the temperature-dependence of the absorption spectrum are used to extract the local optical transition energies of the reaction-center pigments, the so-called site energies, from experimental data. The site energies are verified by calculations and comparison with seven additional independent experiments. Exciton relaxation and primary electron transfer in the reaction center are studied using the site energies. The calculations are used to interpret transient optical data. Evidence is provided for the accessory chlorophyll of the D1-branch as being the primary electron donor and the location of the triplet state at low temperatures.

FIGURE 1

Arrangement of pigments in the PS-II RC. Numbers are the wavelengths in nanometers corresponding to the site energies of the pigments, determined as described in the text. The lower section of the figure contains an additional view on the six core pigments, obtained after a 90° rotation.

FIGURE 2

Absorption (OD), circular dichroism (CD), and fluorescence and linear dichroism (LD) spectra of D1–D2 complexes at 6 K. Solid lines show calculations obtained for the optimized site energies given in Fig. 1. Circles are the experimental data (Germano et al., 2001, 2000).

FIGURE 3

Temperature-dependence of absorption spectra of D1–D2 complexes. Asterisks correspond to the experimental data by Germano et al. (2001) at 6 K, circles show the experiments by Konermann and Holzwarth (1996) at 10 K, 77 K, 150 K, and 277 K, solid lines are the spectra calculated taking into account a temperature-dependence of the site energy of Acc_D1 (678 nm at 6K/10K, 677.5 nm at 77 K, 677 nm at 150 K, and 675 nm at 277 K), and dashed lines are calculations with constant site energy of Acc_D1 (678 nm). The spectra at different temperatures have been shifted vertically by adding a constant for better visibility.

FIGURE 4

10-K triplet-minus-singlet (T-S) spectrum. Circles are experimental values by Germano et al. (2001), solid line is calculation assuming triplet localized at Acc_D1, and dashed line assuming triplet localization at P_D1.

FIGURE 5

(A) 5-K absorption difference spectrum with modified Pheo_D2. Solid line is calculation; circles are experimental values (Germano et al., 2001). (B) 5-K absorption difference spectrum with modified Pheo_D1 and Pheo_D2. Solid line is calculation; circles are experimental values (Germano et al., 2001). (C) 77-K absorption difference spectrum with reduced Pheo_D1. Solid line is calculation, circles are experimental values (Vacha et al., 2002), and dashed line shows calculation without electrochromic shifts. (D) Calculation (solid line) of 10-K absorption difference spectrum with reduced Pheo_D1 and oxidized P_D1, comparison with experimental data (van Kan et al., 1990). (E) 277-K T-S spectrum, circles are experimental values (Durrant et al., 1990), dotted line shows calculation for triplet localized at Acc_D1, dashed line for triplet localized at P_D1, and solid line for a mixture of both according to a thermal population of triplet states (for details, see text). (F) 77-K absorption and difference spectra of RC-6 and RC-5 preparations (for explanation, see text). Solid (RC-6) and dotted (RC-5) lines are calculations, triangles, and circles are experimental values (Vacha et al., 1995); dashed line and squares are theoretical and experimental difference spectra, RC-5−RC-6.

FIGURE 6

Comparison of different theories of linear absorption (explanation is given in the text).

FIGURE 7

Density of exciton states d_M(ω) and exciton states pigment distributions d_m(ω) of the six core pigments.

FIGURE 8

Calculation of disorder averaged exciton lifetimes at 6 K (top) and at room temperature (bottom). (Left) For the six core pigments; (right) including also the two peripheral chlorophylls Chlz_D1, Chlz_D2. Inset (top left) shows subpicosecond lifetimes: τ < 100 fs (dotted line), 100 fs < τ < 500 fs (solid line), and 500 fs < τ < 1 ps (dashed line).

FIGURE 9

Calculation of exciton population decay at 7 K (solid lines) and at room temperature (dashed lines) due to primary electron transfer. (Top) Assuming primary donor is P_D1; (bottom) assuming primary donor is cc_D1.