Förster energy transfer theory as reflected in the structures of photosynthetic light-harvesting systems

Abstract

Förster’s theory of resonant energy transfer underlies a fundamental process in nature, namely the harvesting of sunlight by photosynthetic life forms. The theoretical framework developed by Förster and others describes how electronic excitation migrates in the photosynthetic apparatus of plants, algae, and bacteria from light absorbing pigments to reaction centers where light energy is utilized for the eventual conversion into chemical energy. The demand for highest possible efficiency of light harvesting appears to have shaped the evolution of photosynthetic species from bacteria to plants which, despite a great variation in architecture, display common structural themes founded on the quantum physics of energy transfer as described first by Förster. Herein, Förster’s theory of excitation transfer is summarized, including recent extensions, and the relevance of the theory to photosynthetic systems as evolved in purple bacteria, cyanobacteria, and plants is demonstrated. Förster’s energy transfer formula, as used widely today in many fields of science, is also derived.

Figure 1

Structure of chlorophyll a molecule. The transition dipole moment of the lowest (Q_y) state lies approximately in the plane of the porphyrin ring, along the vector connecting the N_B and N_D atoms.

Figure 2

Pigment organization across different photosynthetic systems. (A) Top view (perpendicular to the membrane plane) and (B) side view (along the membrane plane) of pigment-protein complexes (i to vi) LH2 [42], RC-LH1 monomer [43], RC-LH1 dimer model [69], cyanobacterial PS1 [35], plant PS1 with Lhca subunits [37], and PS2 [38], respectively. Protein components are shown as transparent blue traces to highlight the Chls and BChls (green; shown only as porphyrin rings) and the carotenoids (orange). (See Supplementary Material for movies of these systems.)

Figure 3

Orientations of the transition dipole moments of the constituent BChl and Chl molecules. (A) Top view (perpendicular to the plane of the membrane) and (B) side view (along the plane of the membrane); (i) LH2 [42], (ii) monomeric RC-LH1 [43, 147], and (iii) cyanobacterial PS1 [35].

Figure 4

Structural models for (A) spherical [22, 23], (B) lamellar [121], and (C) tubular [55, 92] photosynthetic chromatophores from purple bacteria. Shown above are the constituent proteins: LH2 complexes (green) and RC-LH1 complexes (LH1 in red; RC in blue). Shown below are the associated BChl networks. The lamellar patch (B) is shown embedded in a lipid membrane, containing a total of nearly 23 million atoms including water (not shown). (See Supplementary Material for movies of these systems.)

Figure 5

The excitation transfer process D*A → DA*. Here, φ_D and φ_A are the ground state orbitals of the donor and acceptor electrons and φ_D* and φ_A* are the excited state orbitals of the donor and acceptor electrons, respectively.

Figure 6

Positions of donor pigment R_D and donor electron r_D and of acceptor pigment R_A and acceptor electron r_A.