Theory of Photosynthetic Energy and Charge Transfer

In photosynthesis carbon dioxid, water and sun light are used to synthesize sugar, which is an important building block of plants. Nature has developed a complicated machinery in order to catalyze this light- driven reaction. Many microscopic details are not fully understood yet. In this project we aim at deciphering the structure-function relationships of the primary energy and charge transfer reactions of photosynthesis. Sun light absorbed in light-harvesting antennae is transferred to the photosynthetic reaction center, where it is used to drive electron transfer reactions. In photosystem II water is split into oxygen, electrons and protons. The oxygen is released, the electrons are shuttled to photosystem I, where they are stored in the chemical bonds of NADPH. The protons drive a molecular motor, the ATPase, which generates ATP, the energy of which is used later in the carbohydrate synthesis. The collection of light energy occurs with a quantum efficiency close to 100 %, that is from 100 absorbed photons on average more than 95 reach the photosynthetic reaction center and drive a chain of primary electron transfer reactions. The latter initiate the chemical reactions for the storage of the solar energy. The origin of the high quantum efficiency of the primary excitation energy and charge transfer reactions is given by the pigment-protein coupling. The optically active pigments (chlorophylls and carotenoids) are held in an optimal distance and orientation for energy- and charge transfer by the protein scaffold. Moreover, the protein also controls the electronic energies of the pigments by electrostatic interactions. In this way, a directed energy transfer towards the reaction center becomes possible. In the present project we want to decipher the underlying molecular details on the basis of the atomic structure of various photosynthetic pigment-protein complexes. In our previous project we have developed a multi- scale approach and investigated the energy transfer in small subunits of the photosynthetic apparatus. Here, we will study the interplay of energy and charge transfer in larger parts of the photosystems. For this purpose, on one hand, it will be necessary to incorporate charge transfer states in our description and on the other hand we need to develop efficient calculation schemes for the description of optical experiments on large systems containing a few hundred pigments. On this basis, we want to understand the molecular building principles of photosynthetic complexes, that will be helpful also in the construction of artificial solar energy converting systems like organic solar cells.

This project was concerned with the development of structure-based theoretical methods for energy transfer and optical spectra of photosynthetic complexes. The challenge is to parameterize the electronic and vibrational degrees of freedom of the system and to describe their light-driven dynamics. In the past, we have begun to develop multiscale methods that combine quantum chemical calculations on isolated pigments with electrostatic and molecular mechanical calculations on the entire pigment-protein complex, which was advanced here in three points: 1) Correlations in the fluctuations of local optical transition energies of the pigments and their role for energy transfer over large distances were investigated. 2) The influence of the polarizable environment on the oscillator strength of the optical transitions was taken into account in the calculation of energy transfer couplings. 3) The influence of short-range effects between neighboring pigments on the parameters of the exciton Hamiltonian and on the local transition dipole moments of the pigments was investigated. New insights into the structure-function relationships of photosystems were obtained: 1) The light-harvesting efficiency of supercomplexes of green sulfur bacteria could be determined on a structural basis. The resulting efficiency of 95 % was found to depend only weakly on the parameterization of the local transition energies of the pigments, but strongly on the relative time scale of energy transfer to the reaction center and electron transfer in the latter. The picture of a flat energy landscape arises with a reaction center that must capture the excitons from the antenna as instantaneously as possible by electron transfer before they can escape back into the antenna. The energy transfer funnel in the FMO protein is needed for photoprotection and not, as previously believed, for a high light-harvesting efficiency. The correlations in excitation energy fluctuations of pigments are much longer-range than the delocalization of excited states, but have no significant influence on energy transfer. 2) In the special pair of photosystem II of higher plants and cyanobacteria, a central chlorophyll dimer, the excitonic coupling is increased by 100 % due to the coupling to charge transfer states , whereas the excited states are hardly lowered in their energy, in contrast to purple bacteria, where both are shifted. We suspect that this change is needed for reaching a high-enough redox potential for water splitting in photosystem II. New insights were obtained into optical line shapes and optical spectroscopy with circularly polarized light. Electron exchange between pigments leads to a slight twisting of the electric dipole moments in relation to the magnetic ones and can be detected with circularly polarized light. A new type of spectroscopy, named time-resolved circular dichroism, was proposed. With this method one can measure energy transfer via states that are dark for linearly polarized light.