• Energy Research

We overview experimental and theoretical studies of energy transfer in the photosynthetic light-harvesting complexes LH1, LH2, and LHCII performed during the past decade since the discovery of high-resolution structure of these complexes. Experimental findings obtained with various spectroscopic techniques makes possible a modelling of the excitation dynamics at a quantitative level. The modified Redfield theory allows a precise assignment of the energy transfer pathways together with a direct visualization of the whole excitation dynamics where various regimes from a coherent motion of delocalized exciton to a hopping of localized excitations are superimposed. In a single complex it is possible to observe the switching between these regimes driven by slow conformational motion (as we demonstrate for LH2). Excitation dynamics under quenched conditions in higher-plant complexes is discussed.

Room temperature absorption difference spectra were measured on the femtosecond through picosecond time scales for chlorosomes isolated from the green bacterium Chloroflexus aurantiacus. Anomalously high values of photoinduced absorption changes were revealed in the BChl c Qy transition band. Photoinduced absorption changes at the bleaching peak in the BChl c band were found to be 7–8 times greater than those at the bleaching peak in the BChl a band of the chlorosome. This appears to be the first direct experimental proof of excitation delocalization over many BChl c antenna molecules in the chlorosome.

Single-molecule spectroscopy was employed to elucidate the fluorescence spectral heterogeneity and dynamics of individual, immobilized trimeric complexes of the main light-harvesting complex of plants in solution near room temperature. Rapid reversible spectral shifts between various emitting states, each of which was quasi-stable for seconds to tens of seconds, were observed for a fraction of the complexes. Most deviating states were characterized by the appearance of an additional, red-shifted emission band. Reversible shifts of up to 75 nm were detected. By combining modified Redfield theory with a disordered exciton model, fluorescence spectra with peaks between 670 nm and 705 nm could be explained by changes in the realization of the static disorder of the pigment-site energies. Spectral bands beyond this wavelength window suggest the presence of special protein conformations. We attribute the large red shifts to the mixing of an excitonic state with a charge-transfer state in two or more strongly coupled chlorophylls. Spectral bluing is explained by the formation of an energy trap before excitation energy equilibration is completed.

Two-dimensional photon echo in the photosystem II reaction center reveals the exciton-vibrational coherences that promote directed energy/electron transfers.

Structure-based calculations are combined with quantitative modeling of spectra and energy transfer dynamics to detemine the energy transfer scheme of the PE545 principal light-harvesting antenna of the cryptomonad Rhodomonas CS24. We use a recently developed quantum-mechanics/molecular mechanics (QM/MM) method that allows us to account for pigment-protein interactions at atomic detail in site energies, transition dipole moments, and electronic couplings. In addition, conformational flexibility of the pigment-protein complex is accounted for through molecular dynamics (MD) simulations. We find that conformational disorder largely smoothes the large energetic differences predicted from the crystal structure between the pseudosymmetric pairs PEB50/61C-PEB50/61D and PEB82C-PEB82D. Moreover, we find that, in contrast to chlorophyll-based photosynthetic complexes, pigment composition and conformation play a major role in defining the energy ladder in the PE545 complex, rather than specific pigment-protein interactions. This is explained by the remarkable conformational flexibility of the eight bilin pigments in PE545, characterized by a quasi-linear arrangement of four pyrrole units. The MD-QM/MM site energies allow us to reproduce the main features of the spectra, and minor adjustments of the energies of the three red-most pigments DBV19A, DBV19B, and PEB82D allow us to model the spectra of PE545 with a similar quality compared to our original model (model E from Novoderezhkin et al. Biophys. J.2010, 99, 344), which was extracted from the spectral and kinetic fit. Moreover, the fit of the transient absorption kinetics is even better in the new structure-based model. The largest difference between our previous and present results is that the MD-QM/MM calculations predict a much smaller gap between the PEB50/61C and PEB50/61D sites, in better accord with chemical intuition. We conclude that the current adjusted MD-QM/MM energies are more reliable in order to explore the spectral properties and energy transfer dynamics in the PE545 complex.

We perform a quantitative comparison of different energy transfer theories, i.e. modified Redfield, standard and generalized Förster theories, as well as combined Redfield-Förster approach. Physical limitations of these approaches are illustrated and critical values of the key parameters indicating their validity are found. We model at a quantitative level the spectra and dynamics in two photosynthetic antenna complexes: in phycoerythrin 545 from cryptophyte algae and in trimeric LHCII complex from higher plants. These two examples show how the structural organization determines a directed energy transfer and how equilibration within antenna subunits and migration between subunits are superimposed.

AbstractWe explain the transient absorption kinetics (E. Romero, I. H. M. van Stokkum, V. I. Novoderezhkin, J. P. Dekker, R. van Grondelle, Biochemistry 2010, 49, 4300) measured for isolated reaction centers of photosystem II at 77 K upon excitation of the primary donor band (680 nm). The excited‐state dynamics is modeled on the basis of the exciton states of 6 cofactors coupled to 4 charge‐transfer (CT) states. One CT state (corresponding to charge separation within the special pair) is supposed to be strongly coupled with the excited states, whereas the other radical pairs are supposed to be localized. Relaxation within the strongly coupled manifold and transfer to localized CT’s are described by the modified Redfield and generalized Förster theories, respectively. A simultaneous and quantitative fit of the 680, 545, and 460 nm kinetics (corresponding to respectively the Qy transitions of the red‐most cofactors, Qx transition of pheophytin, and pheophytin anion absorption) enables us to define the pathways and time scales of primary electron transfer. A consistent modeling of the data is only possible with a Scheme where charge separation occurs from both the accessory chlorophyll and from the special pair, giving rise to fast and slow components of the pheophytin anion formation, respectively.

We model the spectra (absorption and circular dichroism) and excitation dynamics in the B800 ring of the LH2 antenna complex from Rs. molischianum using different theoretical approaches, i.e., Förster theory, standard and modified versions of the Redfield theory, and the more versatile nonperturbative approach based on hierarchically coupled equations for the reduced density operator. We demonstrate that, although excitations in the B800 ring are localized due to disorder, thermal effects, and phonons, there are still sizable excitonic effects producing shift, narrowing, and asymmetry of the spectra. Moreover, the excitation dynamics reveals the presence of long-lived (up to 1 ps) non-oscillatory coherences between the exciton states maintained due to nonsecular population-to-coherence transfers. The sub-ps decay of the coherences is followed by slow motion of the excitation around the ring, producing equilibration of the site populations with a time constant of about 3-4 ps, which is slower than the B800 → B850 transfer. The exact solution obtained with the hierarchical equations is compared with other approaches, thus illustrating limitations of the Förster and Redfield pictures.