Preferential pathways for light-trapping involving β-ligated chlorophylls

AbstractThe magnesium atom of chlorophylls (Chls) is always five- or six-coordinated within chlorophyll–protein complexes which are the main light-harvesting systems of plants, algae and most photosynthetic bacteria. Due to the presence of stereocenters and the axial ligation of magnesium the two faces of Chls are diastereotopic. It has been previously recognized that the α-configuration having the magnesium ligand on the opposite face of the 17-propionic acid moiety is more frequently encountered and is more stable than the more seldom β-configuration that has the magnesium ligand on the same face [T.S. Balaban, P. Fromme, A.R. Holzwarth, N. Krauβ, V.I. Prokhorenko, Relevance of the diastereotopic ligation of magnesium atoms in chlorophylls in Photosystem I, Biochim. Biophys. Acta (Bioenergetics), 1556 (2002) 197–207; T. Oba, H. Tamiaki, Which side of the π-macrocycle plane of (bacterio)chlorophylls is favored for binding of the fifth ligand? Photosynth. Res. 74 (2002) 1–10]. In photosystem I only 14 Chls out of a total of 96 are in a β-configuration and these occupy preferential positions around the reaction center. We have now analyzed the α/β dichotomy in the homodimeric photosystem II based on the 2.9 Å resolution crystal structure [A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, W. Saenger, Cyanobacterial photosystem II at 2.9 Å resolution: role of quinones, lipids, channels and chloride, Nature Struct. Mol. Biol. 16 (2009) 334–342] and find that out of 35 Chls in each monomer only 9 are definitively in the β-configuration, while 4 are uncertain. Ab initio calculations using the approximate coupled-cluster singles-and-doubles model CC2 [O. Christiansen, H. Koch, P. Jørgensen, The second-order approximate coupled cluster singles and doubles model CC2, Chem. Phys. Lett. 243 (1995) 409–418] now correctly predict the absorption spectra of Chls a and b and conclusively show for histidine, which is the most frequent axial ligand of magnesium in chlorophyll–protein complexes, that only slight differences (<4 nm) are encountered between the α- and β-configurations. Significant red shifts (up to 50 nm) can, however, be encountered in excitonically coupled β–β-Chl dimers. Surprisingly, in both photosystems I and II very similar “special” β–β dimers are encountered at practically the same distances from P700 and P680, respectively. In purple bacteria LH2, the B850 ring is composed exclusively of such tightly coupled β-bacteriochlorophylls a. A statistical analysis of the close contacts with the protein matrix (<5 Å) shows significant differences between the α- and β-configurations and the subunit providing the axial magnesium ligand. The present study allows us to conclude that the excitation energy transfer in light-harvesting systems, from a peripheral antenna towards the reaction center, may follow preferential pathways due to structural reasons involving β-ligated Chls

Polarization charge densities provide a predictive quantification of hydrogen bond energies

A systematic density functional theory based study of hydrogen bond energies of 2465 single hydrogen bonds has been performed. In order to be closer to liquid phase conditions, different from the usual reference state of individual donor and acceptor molecules in vacuum, the reference state of donors and acceptors embedded in a perfect conductor as simulated by the COSMO solvation model has been used for the calculation of the hydrogen bond energies. The relationship between vacuum and conductor reference hydrogen bond energies is investigated and interpreted in the light of different physical contributions, such as electrostatic energy and dispersion. A very good correlation of the DFT/COSMO hydrogen bond energies with conductor polarization charge densities of separated donor and acceptor atoms was found. This provides a method to predict hydrogen bond strength in solution with a root mean square error of 0.36 kcal mol−1 relative to the quantum chemical dimer calculations. The observed correlation is broadly applicable and allows for a predictive quantification of hydrogen bonding, which can be of great value in many areas of computational, medicinal and physical chemistry