On uncorrelated inter-monomer Förster energy transfer in Fenna-Matthews-Olson complexes.

The Fenna-Matthews-Olson (FMO) light-harvesting antenna protein of green sulfur bacteria is a long-studied pigment-protein complex which funnels energy from the chlorosome to the reaction centre where photochemistry takes place. The structure of the FMO protein from Chlorobaculum tepidum is known as a homotrimeric complex containing eight bacteriochlorophyll a per monomer. Owing to this structure FMO has strong intra-monomer and weak inter-monomer electronic coupling constants. While long-lived (sub-picosecond) coherences within a monomer have been a prevalent topic of study over the past decade, various experimental evidence supports the presence of subsequent inter-monomer energy transfer on a picosecond time scale. The latter has been neglected by most authors in recent years by considering only sub-picosecond time scales or assuming that the inter-monomer coupling between low-energy states is too weak to warrant consideration of the entire trimer. However, Förster theory predicts that energy transfer of the order of picoseconds is possible even for very weak (less than 5 cm-1) electronic coupling between chromophores. This work reviews experimental data (with a focus on emission and hole-burned spectra) and simulations of exciton dynamics which demonstrate inter-monomer energy transfer. It is shown that the lowest energy 825 nm absorbance band cannot be properly described by a single excitonic state. The energy transfer through FMO is modelled by generalized Förster theory using a non-Markovian, reduced density matrix approach to describe the electronic structure. The disorder-averaged inter-monomer transfer time across the 825 nm band is about 27 ps. While only isolated FMO proteins are presented, the presence of inter-monomer energy transfer in the context of the overall photosystem is also briefly discussed.

Primary light-energy conversion in tetrameric chlorophyll structure of photosystem II and bacterial reaction centers: I. A review.

The purpose of the review is to show that the tetrameric (bacterio)chlorophyll ((B)Chl) structures in reaction centers of photosystem II (PSII) of green plants and in bacterial reaction centers (BRCs) are similar and play a key role in the primary charge separation. The Stark effect measurements on PSII reaction centers have revealed an increased dipole moment for the transition at approximately 730 nm (Frese et al., Biochemistry 42:9205-9213, 2003). It was found (Heber and Shuvalov, Photosynth Res 84:84-91, 2005) that two fluorescent bands at 685 and 720 nm are observed in different organisms. These two forms are registered in the action spectrum of Q(A) photoreduction. Similar results were obtained in core complexes of PSII at low temperature (Hughes et al., Biochim Biophys Acta 1757: 841-851, 2006). In all cases the far-red absorption and emission can be interpreted as indication of the state with charge transfer character in which the chlorophyll monomer plays a role of an electron donor. The role of bacteriochlorophyll monomers (B(A) and B(B)) in BRCs can be revealed by different mutations of axial ligand for Mg central atoms. RCs with substitution of histidine L153 by tyrosine or leucine and of histidine M182 by leucine (double mutant) are not stable in isolated state. They were studied in antennaless membrane by different kinds of spectroscopy including one with femtosecond time resolution. It was found that the single mutation (L153HY) was accompanied by disappearance of B(A) molecule absorption near 802 nm and by 14-fold decrease of photochemical activity measured with ms time resolution. The lifetime of P(870)* increased up to approximately 200 ps in agreement with very low rate of the electron transfer to A-branch. In the double mutant L153HY + M182HL, the B(A) appears to be lost and B(B) is replaced by bacteriopheophytin Phi(B) with the absence of any absorption near 800 nm. Femtosecond measurements have revealed the electron transfer to B-branch with a time constant of approximately 2 ps. These results are discussed in terms of obligatory role of B(A) and Phi(B) molecules located near P for efficient electron transfer from P*.