Vladimir I. Novoderezhkin

Energy transfer in photosynthesis: experimental insights and quantitative models.

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.

Quantum coherence in photosynthesis for efficient solar-energy conversion

The crucial step in the conversion of solar to chemical energy in Photosynthesis takes place in the reaction center where the absorbed excitation energy is converted into a stable charge separated state by ultrafast electron transfer events. However, the fundamental mechanism responsible for the near unity quantum efficiency of this process is unknown. Here we elucidate the role of coherence in determining the efficiency of charge separation in the plant photosystem II reaction centre (PSII RC) by comprehensively combining experiment (two-dimensional electronic spectroscopy) and theory (Redfield theory). We reveal the presence of electronic coherence between excitons as well as between exciton and charge transfer states which we argue to be maintained by vibrational modes. Furthermore, we present evidence for the strong correlation between the degree of electronic coherence and efficient and ultrafast charge separation. We propose that this coherent mechanism will inspire the development of new energy technologies.

Physical origins and models of energy transfer in photosynthetic light-harvesting

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.

Fluorescence Spectral Dynamics of Single LHCII Trimers

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 Different Charge Separation Pathways in Photosystem II

Charge separation is an essential step in the conversion of solar energy into chemical energy in photosynthesis. To investigate this process, we performed transient absorption experiments at 77 K with various excitation conditions on the isolated Photosystem II reaction center preparations from spinach. The results have been analyzed by global and target analysis and demonstrate that at least two different excited states, (Chl(D1)Phe(D1))* and (P(D1)P(D2)Chl(D1))*, give rise to two different pathways for ultrafast charge separation. We propose that the disorder produced by slow protein motions causes energetic differentiation among reaction center complexes, leading to different charge separation pathways. Because of the low temperature, two excitation energy trap states are also present, generating charge-separated states on long time scales. We conclude that these slow trap states are the same as the excited states that lead to ultrafast charge separation, indicating that at 77 K charge separation can be either activation-less and fast or activated and slow.

Multiple Charge‐Separation Pathways in Photosystem II: Modeling of Transient Absorption Kinetics

We 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 CTs 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 Q(y) transitions of the red-most cofactors, Q(x) 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.

Excitonic interactions in the light-harvesting antenna of photosynthetic purple bacteria and their influence on picosecond absorbance difference spectra

A new model of the light‐harvesting antenna (core complex) of purple photosynthetic bacteria is proposed based on excitonic interactions in circular aggregates of bacteriochlorophyll molecules. The calculated absorbance difference spectra of circular aggregates demonstrate all special features observed in the experimental spectra of purple bacteria. In particular, the absorption changes with high amplitude of bleaching at the longwavelength side of the absorption band at different excitation energy are predicted.

Disordered Exciton Model for the Core Light-Harvesting Antenna of Rhodopseudomonas viridis

In this work we explain the spectral heterogeneity of the absorption band (. Biochim. Biophys. Acta. 1229:373-380), as well as the spectral evolution of pump-probe spectra for membranes of Rhodopseudomonas (Rps.) viridis. We propose an exciton model for the LH1 antenna of Rps. viridis and assume that LH1 consists of 24-32 strongly coupled BChl b molecules that form a ring-like structure with a 12- or 16-fold symmetry. The orientations and pigment-pigment distances of the BChls were taken to be the same as for the LH2 complexes of BChl a-containing bacteria. The model gave an excellent fit to the experimental results. The amount of energetic disorder necessary to explain the results could be precisely estimated and gave a value of 440-545 cm(-1) (full width at half-maximum) at low temperature and 550-620 cm(-1) at room temperature. Within the context of the model we calculated the coherence length of the steady-state exciton wavepacket to correspond to a delocalization over 5-10 BChl molecules at low temperature and over 4-6 molecules at room temperature. Possible origins of the fast electronic dephasing and the observed long-lived vibrational coherence are discussed.

Quantum design of photosynthesis for bio-inspired solar-energy conversion

Photosynthesis is the natural process that converts solar photons into energy-rich products that are needed to drive the biochemistry of life. Two ultrafast processes form the basis of photosynthesis: excitation energy transfer and charge separation. Under optimal conditions, every photon that is absorbed is used by the photosynthetic organism. Fundamental quantum mechanics phenomena, including delocalization, underlie the speed, efficiency and directionality of the charge-separation process. At least four design principles are active in natural photosynthesis, and these can be applied practically to stimulate the development of bio-inspired, human-made energy conversion systems.

Energy Transfer in Light-Harvesting Complexes LHCII and CP29 of Spinach Studied with Three Pulse Echo Peak Shift and Transient Grating

Three pulse echo peak shift and transient grating (TG) measurements on the plant light-harvesting complexes LHCII and CP29 are reported. The LHCII complex is by far the most abundant light-harvesting complex in higher plants and fulfills several important physiological functions such as light-harvesting and photoprotection. Our study is focused on the light-harvesting function of LHCII and the very similar CP29 complex and reveals hitherto unresolved excitation energy transfer processes. All measurements were performed at room temperature using detergent isolated complexes from spinach leaves. Both complexes were excited in their Chl b band at 650 nm and in the blue shoulder of the Chl a band at 670 nm. Exponential fits to the TG and three pulse echo peak shift decay curves were used to estimate the timescales of the observed energy transfer processes. At 650 nm, the TG decay can be described with time constants of 130 fs and 2.2 ps for CP29, and 300 fs and 2.8 ps for LHCII. At 670 nm, the TG shows decay components of 230 fs and 6 ps for LHCII, and 300 fs and 5 ps for CP29. These time constants correspond to well-known energy transfer processes, from Chl b to Chl a for the 650 nm TG and from blue (670 nm) Chl a to red (680 nm) Chl a for the 670 nm TG. The peak shift decay times are entirely different. At 650 nm we find times of 150 fs and 0.5-1 ps for LHCII, and 360 fs and 3 ps for CP29, which we can associate mainly with Chl b <--> Chl b energy transfer. At 670 nm we find times of 140 fs and 3 ps for LHCII, and 3 ps for CP29, which we can associate with fast (only in LHCII) and slow transfer between relatively blue Chls a or Chl a states. From the occurrence of both fast Chl b <--> Chl b and fast Chl b --> Chl a transfer in CP29, we conclude that at least two mixed binding sites are present in this complex. A detailed comparison of our observed rates with exciton calculations on both CP29 and LHCII provides us with more insight in the location of these mixed sites. Most importantly, for CP29, we find that a Chl b pair must be present in some, but not all, complexes, on sites A(3) and B(3). For LHCII, the observed rates can best be understood if the same pair, A(3) and B(3), is involved in both fast Chl b <--> Chl b and fast Chl a <--> Chl a transfer. Hence, it is likely that mixed sites also occur in the native LHCII complex. Such flexibility in chlorophyll binding would agree with the general flexibility in aggregation form and xanthophyll binding of the LHCII complex and could be of use for optimizing the role of LHCII under specific circumstances, for example under high-light conditions. Our study is the first to provide spectroscopic evidence for mixed binding sites, as well as the first to show their existence in native complexes.