Andrius Gelzinis

Vibronic coherence in oxygenic photosynthesis

Photosynthesis powers life on our planet. The basic photosynthetic architecture consists of antenna complexes that harvest solar energy and reaction centres that convert the energy into stable separated charge. In oxygenic photosynthesis, the initial charge separation occurs in the photosystem II reaction centre, the only known natural enzyme that uses solar energy to split water. Both energy transfer and charge separation in photosynthesis are rapid events with high quantum efficiencies. In recent nonlinear spectroscopic experiments, long-lived coherences have been observed in photosynthetic antenna complexes, and theoretical work suggests that they reflect underlying electronic-vibrational resonances, which may play a functional role in enhancing energy transfer. Here, we report the observation of coherent dynamics persisting on a picosecond timescale at 77 K in the photosystem II reaction centre using two-dimensional electronic spectroscopy. Supporting simulations suggest that the coherences are of a mixed electronic-vibrational (vibronic) nature and may enhance the rate of charge separation in oxygenic photosynthesis.

Tight-binding model of the photosystem II reaction center: application to two-dimensional electronic spectroscopy

We propose an optimized tight-binding electron-hole model of the photosystem II (PSII) reaction center (RC). Our model incorporates two charge separation pathways and spatial correlations of both static disorder and fast fluctuations of energy levels. It captures the main experimental features observed in time-resolved two-dimensional (2D) optical spectra at 77K: peak pattern, lineshapes and time traces. Analysis of 2D spectra kinetics reveals that specific regions of the 2D spectra of the PSII RC are sensitive to the charge transfer states. We find that the energy disorder of two peripheral chlorophylls is four times larger than the other RC pigments.

The nature of self-regulation in photosynthetic light-harvesting antenna

The photosynthetic apparatus of green plants is well known for its extremely high efficiency that allows them to operate under dim light conditions. On the other hand, intense sunlight may result in overexcitation of the light-harvesting antenna and the formation of reactive compounds capable of ‘burning out’ the whole photosynthetic unit. Non-photochemical quenching is a self-regulatory mechanism utilized by green plants on a molecular level that allows them to safely dissipate the detrimental excess excitation energy as heat. Although it is believed to take place in the plants major light-harvesting complexes (LHC) II, there is still no consensus regarding its molecular nature. To get more insight into its physical origin, we performed high-resolution time-resolved fluorescence measurements of LHCII trimers and their aggregates across a wide temperature range. Based on simulations of the excitation energy transfer in the LHCII aggregate, we associate the red-emitting state, having fluorescence maximum at ∼700 nm, with the partial mixing of excitonic and chlorophyll–chlorophyll charge transfer states. On the other hand, the quenched state has a totally different nature and is related to the incoherent excitation transfer to the short-lived carotenoid excited states. Our results also show that the required level of photoprotection in vivo can be achieved by a very subtle change in the number of LHCIIs switched to the quenched state.

Excitation dynamics and relaxation in a molecular heterodimer

Abstract The exciton dynamics in a molecular heterodimer is studied as a function of differences in excitation and reorganization energies, asymmetry in transition dipole moments and excited state lifetimes. The heterodimer is composed of two molecules modeled as two-level systems coupled by the resonance interaction. The system-bath coupling is taken into account as a modulating factor of the molecular excitation energy gap, while the relaxation to the ground state is treated phenomenologically. Comparison of the description of the excitation dynamics modeled using either the Redfield equations (secular and full forms) or the Hierarchical quantum master equation (HQME) is demonstrated and discussed. Possible role of the dimer as an excitation quenching center in photosynthesis self-regulation is discussed. It is concluded that the system-bath interaction rather than the excitonic effect determines the excitation quenching ability of such a dimer.

Mapping energy transfer channels in fucoxanthin-chlorophyll protein complex.

Fucoxanthin-chlorophyll protein (FCP) is the key molecular complex performing the light-harvesting function in diatoms, which, being a major group of algae, are responsible for up to one quarter of the total primary production on Earth. These photosynthetic organisms contain an unusually large amount of the carotenoid fucoxanthin, which absorbs the light in the blue-green spectral region and transfers the captured excitation energy to the FCP-bound chlorophylls. Due to the large number of fucoxanthins, the excitation energy transfer cascades in these complexes are particularly tangled. In this work we present the two-color two-dimensional electronic spectroscopy experiments on FCP. Analysis of the data using the modified decay associated spectra permits a detailed mapping of the excitation frequency dependent energy transfer flow with a femtosecond time resolution.

Dynamics of exciton-polaron transition in molecular assemblies: The variational approach

Dynamics of excitonic polaron formation in molecular systems coupled to an overdamped bath are investigated using the Dirac-Frenkel variational principle and Davydov D1 Ansatz. Using a two-site model system we show that a few qualitatively distinct relaxation regimes of an optically created exciton are possible, depending on the timescale of bath fluctuations. A slow bath always leads to adiabatic polaron formation. Non-adiabatic exciton self-trapping occurs when the system is strongly coupled to a fast bath. Weak coupling to such bath does not perturb the excitonic picture. The complex system-bath dynamics can then be mapped to an effective model where the resonant coupling between sites is quenched during relaxation. The timescale of the polaron formation can be defined by the timescale of resonant coupling quenching, and is found to directly correlate with the bath relaxation time.

Coherence and population dynamics of chlorophyll excitations in FCP complex: Two-dimensional spectroscopy study

Energy transfer processes and coherent phenomena in the fucoxanthin-chlorophyll protein complex, which is responsible for the light harvesting function in marine algae diatoms, were investigated at 77 K by using two-dimensional electronic spectroscopy. Experiments performed on femtosecond and picosecond timescales led to separation of spectral dynamics, witnessing evolutions of coherence and population states of the system in the spectral region of Qy transitions of chlorophylls a and c. Analysis of the coherence dynamics allowed us to identify chlorophyll (Chl) a and fucoxanthin intramolecular vibrations dominating over the first few picoseconds. Closer inspection of the spectral region of the Qy transition of Chl c revealed previously not identified, mutually non-interacting chlorophyll c states participating in femtosecond or picosecond energy transfer to the Chl a molecules. Consideration of separated coherent and incoherent dynamics allowed us to hypothesize the vibrations-assisted coherent energy transfer between Chl c and Chl a and the overall spatial arrangement of chlorophyll molecules.

Excitation Energy Transfer and Quenching in a Heterodimer: Applications to the Carotenoid–Phthalocyanine Dyads

The dynamics of a molecular heterodimer composed of a long-lived excitation donor and a short-lived acceptor (quencher) is examined. In order to consider various dynamical regimes without any restrictions on the system parameters, the energy transfer is modeled employing the hierarchical equations of motion, while the relaxation to the ground state is treated by assuming a phenomenological spontaneous nonradiative decay rate. Time scales of the resulting two-exponential evolution are investigated as functions of the energy gap and the resonance coupling between the monomeric constituents of the dimer. Relevance of the present analysis to the recent experimental findings on artificial carotenoid-phthalocyanine dyads is discussed. By examining the first two time scales of the reported time-resolved spectra, it is shown that upon the increase of carotenoid conjugation length its first excited state approaches the first excited state of phthalocyanine from above, thereby inducing a remarkable quenching. The proposed model also provides a unified treatment of quenching in the regimes previously distinguished as energy transfer and excitonic state formation.

Absorption lineshapes of molecular aggregates revisited

Linear absorption is the most basic optical spectroscopy technique that provides information about the electronic and vibrational degrees of freedom of molecular systems. In simulations of absorption lineshapes, often diagonal fluctuations are included using the cumulant expansion, and the off-diagonal fluctuations are accounted for either perturbatively, or phenomenologically. The accuracy of these methods is limited and their range of validity is still questionable. In this work, a systematic study of several such methods is presented by comparing the lineshapes with exact results. It is demonstrated that a non-Markovian theory for off-diagonal fluctuations, termed complex time dependent Redfield theory, gives good agreement with exact lineshapes over a wide parameter range. This theory is also computationally efficient. On the other hand, accounting for the off-diagonal fluctuations using the modified Redfield lifetimes was found to be inaccurate.

Spectroscopic properties of photosystem II reaction center revisited

Photosystem II (PSII) is the only biological system capable of splitting water to molecular oxygen. Its reaction center (RC) is responsible for the primary charge separation that drives the water oxidation reaction. In this work, we revisit the spectroscopic properties of the PSII RC using the complex time-dependent Redfield (ctR) theory for optical lineshapes [A. Gelzinis et al., J. Chem. Phys. 142, 154107 (2015)]. We obtain the PSII RC model parameters (site energies, disorder, and reorganization energies) from the fits of several spectra and then further validate the model by calculating additional independent spectra. We obtain good to excellent agreement between theory and calculations. We find that overall our model is similar to some of the previous asymmetric exciton models of the PSII RC. On the other hand, our model displays differences from previous work based on the modified Redfield theory. We extend the ctR theory to describe the Stark spectrum and use its fit to obtain the parameters of a single charge transfer state included in our model. Our results suggest that ChlD1+PheoD1- is most likely the primary charge transfer state, but that the Stark spectrum of the PSII RC is probably also influenced by other states.