An accurate and numerically efficient method for the calculation of intermolecular Coulomb couplings between charge densities of electronic states and between transition densities of electronic excitations is presented. The coupling of transition densities yields the Förster type excitation energy transfer coupling, and from the charge density coupling, a shift in molecular excitation energies results. Starting from an ab initio calculation of the charge and transition densities, atomic partial charges are determined such as to fit the resulting electrostatic potentials of the different states and the transition. The different intermolecular couplings are then obtained from the Coulomb couplings between the respective atomic partial charges. The excitation energy transfer couplings obtained in the present TrEsp (transition charge from electrostatic potential) method are compared with couplings obtained from the simple point-dipole and extended dipole approximations and with those from the ab initio transition density cube method of Krüger, Scholes, and Fleming. The present method is of the same accuracy as the latter but computationally more efficient. The method is applied to study strongly coupled pigments in the light-harvesting complexes of green sulfur bacteria (FMO), purple bacteria (LH2), and higher plants (LHC-II) and the "special pairs" of bacterial reaction centers and reaction centers of photosystems I and II. For the pigment dimers in the antennae, it is found that the mutual orientation of the pigments is optimized for maximum excitonic coupling. A driving force for this orientation is the Coulomb coupling between ground-state charge densities. In the case of excitonic couplings in the "special pairs", a breakdown of the point-dipole approximation is found for all three reaction centers, but the extended dipole approximation works surprisingly well, if the extent of the transition dipole is chosen larger than assumed previously. For the "special pairs", a large shift in local transition energies is found due to charge density coupling.

The Fenna-Matthews-Olson (FMO) light-harvesting protein connects the outer antenna system (chlorosome/baseplate) with the reaction center complex in green sulfur bacteria. Since its first structure determination in the mid-70s, this pigment-protein complex has become an important model system to study excitation energy transfer. Recently, an additional bacteriochlorophyll a (the eighth) pigment was discovered in each subunit of this homotrimer. Our structure-based calculations of the optical properties of the FMO protein demonstrate that the eighth pigment is the linker to the baseplate, confirming recent suggestions from crystallographic studies.

Optical line shape theory is combined with a quantum-chemical/electrostatic calculation of the site energies of the 96 chlorophyll a pigments and their excitonic couplings to simulate optical spectra of photosystem I core complexes from Thermosynechococcus elongatus. The absorbance, linear dichroism and circular dichroism spectra, calculated on the basis of the 2.5 A crystal structure, match the experimental data semiquantitatively allowing for a detailed analysis of the pigment-protein interaction. The majority of site energies are determined by multiple interactions with a large number (>20) of amino acid residues, a result which demonstrates the importance of long-range electrostatic interactions. The low-energy exciton states of the antenna are found to be located at a nearest distance of about 25 A from the special pair of the reaction center. The intermediate pigments form a high-energy bridge, the site energies of which are stabilized by a particularly large number (>100) of amino acid residues. The concentration of low energy exciton states in the antenna is larger on the side of the A-branch of the reaction center, implying an asymmetric delivery of excitation energy to the latter. This asymmetry in light-harvesting may provide the key for understanding the asymmetric use of the two branches in primary electron transfer reactions. Experiments are suggested to check for this possibility.

The Fenna-Matthews-Olson (FMO) protein of green sulfur bacteria represents an important model protein for the study of elementary pigment-protein couplings. We have previously used a simple approach [Adolphs and Renger (2006) Biophys J 91:2778-2797] to study the shift in local transition energies (site energies) of the FMO protein of Prosthecochloris aestuarii by charged amino acid residues, assuming a standard protonation pattern of the titratable groups. Recently, we have found strong evidence that besides the charged amino acids also the neutral charge density of the protein is important, by applying a combined quantum chemical/electrostatic approach [Müh et al. (2007) Proc Natl Acad Sci USA, in press]. Here, we extract the essential parts from this sophisticated method to obtain a relatively simple method again. It is shown that the main contribution to the site energy shifts is due to charge density coupling (CDC) between the pigments and their pigment, protein and water surroundings and that polarization effects for qualitative considerations can be approximated by screening the Coulomb coupling by an effective dielectric constant.