Quantum mechanical analysis of excitation energy transfer couplings in photosystem II

Abstract

We evaluated excitation energy transfer (EET) coupling (J) between all pairs of chlorophylls (Chls) and pheophytins (Pheos) in the protein environment of photosystem II based on the time-dependent density functional theory with a quantum mechanical/molecular mechanics approach. In the reaction center, the EET coupling between Chls P_D1 and P_D2 is weaker (|J(P_D1/P_D2)| = 79 cm^-1), irrespective of a short edge-to-edge distance of 3.6 Å (Mg-to-Mg distance of 8.1 Å), than the couplings between P_D1 and the accessory Chl_D1 (|J(P_D1/Chl_D2)| = 104 cm^-1) and between P_D2 and Chl_D2 (|J(P_D2/Chl_D1)| = 101 cm^-1), suggesting that P_D1 and P_D2 are two monomeric Chls rather than a "special pair". There exist strongly coupled Chl pairs (|J| > ∼100 cm^-1) in the CP47 and CP43 core antennas, which may be candidates for the red-shifted Chls observed in spectroscopic studies. In CP47 and CP43, Chls ligated to CP47-His26 and CP43-His56, which are located in the middle layer of the thylakoid membrane, play a role in the "hub" that mediates the EET from the lumenal to stromal layers. In the stromal layer, Chls ligated to CP47-His466, CP43-His441, and CP43-His444 mediate the EET from CP47 to Chl_D2/Pheo_D2 and from CP43 to Chl_D1/Pheo_D1 in the reaction center. Thus, the excitation energy from both CP47 and CP43 can always be utilized for the charge-separation reaction in the reaction center.

Figure 1

Schematic illustration of EET. Schematic of (a) EET from the light-harvesting complex to the reaction center in photosynthesis, (b) EET reaction from a donor molecule (D) to an acceptor molecule (A), and its (c) Coulomb and (d) exchange mechanisms (4). A^∗ and D^∗ represent the excited states of A and D molecules, respectively. Black arrows indicate the motion of electrons during EET. The waves represent the Coulomb interactions between the electrons. To see this figure in color, go online.

Figure 2

Geometric configurations of transition dipole moments of the donor (μ_D; red arrow) and acceptor (μ_A; blue solid and dotted arrows). R_DA is the inter-molecular center-to-center distance between the donor and acceptor chromophores. α_AD is the angle between the two transition dipole moments. β_D is the angle between μ_D and R_DA and β_A is the angle between μ_A and R_DA. To see this figure in color, go online.

Figure 3

Arrangement of Chls and Pheos in the PSII core complex. Chls (green) and Pheos (orange) are shown (a) parallel and (b) perpendicular to the thylakoid membrane based on PDB code 3ARC (15). The stromal, middle, and lumenal layers in CP47 and CP43 are indicated by red, cyan, and blue boxes, respectively. The reaction center contains the accessory Chl_D1/Chl_D2, the central Chl dimer P_D1/P_D2, Pheo_D1/Pheo_D2, and Mn₄CaO₅ cluster. Light energy captured by CP47 and CP43 is transferred to the reaction center (orange arrows) via EET and induces a charge separation between P_D1/P_D2 and Pheo_D1; this is followed by subsequent electron transfers from Pheo_D1 to a quinone Q_B (blue arrows). The electron hole on the P_D1/P_D2 pair is reduced by the electron transferred from the Mn₄CaO₅ cluster (black arrow). To see this figure in color, go online.

Figure 4

Geometric configurations of two Chls. R_DA, Mg-Mg distance; d, edge-to-edge distance between chlorine rings; and ϕ, angle between the chlorine planes. To see this figure in color, go online.

Figure 5

Sequence alignment of CP43 and CP47 from T. vulcanus with the axial ligands of Chls, His (yellow) and Asn (green), hydrogen-bond (H-bond) acceptor of the ligand water cluster of Chl (cyan), and transmembrane helix regions (gray), obtained using Clustal (77). The boxed numbers indicate Chls defined in Table 1. Bracketed Chls are not conserved between CP43 and CP47. To see this figure in color, go online.

Figure 6

EET coupling network (|J| >10 cm⁻¹). View from the field (a) parallel and (b) perpendicular to the membrane. Color and width of the lines indicate the magnitude of J. The Chl number corresponds to that in Table 1 (the blue bracketed number indicates Chl existing only in CP47). The boxed picture shows EET coupling, J_dipol, calculated by the dipole approximation. To see this figure in color, go online.

Figure 7

Distribution of the EET interaction J between Chls in the lumenal layer (blue arrow), Chls in the stromal layer (red arrow), middle-layer Chl (CP47-13/CP43-13) and lumenal or stromal Chls (light-brown arrow), lumenal Chls and stromal Chls (purple arrow), and core-antenna Chls and reaction-center Chls (black arrow). (a) Conceptual illustration of the classification of Chl pairs. (b) Distributions in CP47. (c) Distributions in CP43. Values greater than the vertical scale are shown in parentheses. To see this figure in color, go online.

Figure 8

Arrangement of P_D1, P_D2, and Chl_D2. Chlorine planes of P_D1 and P_D2 are arranged in a parallel manner (angle between the chlorine planes, ϕ = ∼0°), whereas those of P_D1 and Chl_D2 are arranged in a non-parallel manner (ϕ = ∼60°). To see this figure in color, go online.

Figure 9

Strongly coupled Chl pairs that are candidates of red Chls. The proposed red Chls (CP43-7 (26,40,52), 10 (26,37,40), and 12 (26,37,40), and CP47-16 (37)) are colored in red. To see this figure in color, go online.

Figure 10

EET pathways and the charge-separation reaction in PSII. View from the field (a) parallel and (b) perpendicular to the membrane. The middle-layer Chls of CP47-13 and CP43-13 connect network between the lumenal and stromal layers. The excitation energy from CP47-8 and CP43-8/11 in the stromal layer reaches the reaction center (red arrows). Because Chl_D1/P_D2 and Chl_D2/P_D1 are strongly coupled (yellow line) compared with the P_D1/P_D2 pair (green line), the excitation energy on Chl_D2 can be transferred to Chl_D1 via P_D1 (black arrow); thus, it is used for the charge-separation reaction on Chl_D1(20) (blue arrows). To see this figure in color, go online.