Electronic coherence transfer in photosynthetic complexes and its signatures in optical spectroscopy (original) (raw)
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Scientific Reports, 2013
A vibronic-exciton model is applied to investigate the recently proposed mechanism of enhancement of coherent oscillations due to mixing of electronic and nuclear degrees of freedom. We study a dimer system to elucidate the role of resonance coupling, site energies, vibrational frequency and energy disorder in the enhancement of vibronic-exciton and ground-state vibrational coherences, and to identify regimes where this enhancement is significant. For a heterodimer representing two coupled bachteriochloropylls of the FMO complex, long-lived vibronic coherences are found to be generated only when the frequency of the mode is in the vicinity of the electronic energy difference. Although the vibronic-exciton coherences exhibit a larger initial amplitude compared to the ground-state vibrational coherences, we conclude that, due to the dephasing of the former, both type of coherences have a similar magnitude at longer population time.
Exciton dynamics in photosynthetic complexes: excitation by coherent and incoherent light
New Journal of Physics, 2010
In this paper we consider dynamics of a molecular system subjected to external pumping by a light source. Within a completely quantum mechanical treatment, we derive a general formula, which enables to asses effects of different light properties on the photo-induced dynamics of a molecular system. We show that once the properties of light are known in terms of certain two-point correlation function, the only information needed to reconstruct the system dynamics is the reduced evolution superoperator. The later quantity is in principle accessible through ultrafast non-linear spectroscopy. Considering a direct excitation of a small molecular antenna by incoherent light we find that excitation of coherences is possible due to overlap of homogeneous line shapes associated with different excitonic states. In Markov and secular approximations, the amount of coherence is significant only under fast relaxation, and both the populations and coherences between exciton states become static at long time. We also study the case when the excitation of a photosynthetic complex is mediated by a mesoscopic system. We find that such case can be treated by the same formalism with a special correlation function characterizing ultrafast fluctuations of the mesoscopic system. We discuss bacterial chlorosom as an example of such a mesoscopic mediator and propose that the properties of energy transferring chromophore-protein complexes might be specially tuned for the fluctuation properties of their associated antennae.
Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems
Nature, 2007
Photosynthetic complexes are exquisitely tuned to capture solar light efficiently, and then transmit the excitation energy to reaction centres, where long term energy storage is initiated. The energy transfer mechanism is often described by semiclassical models that invoke 'hopping' of excited-state populations along discrete energy levels 1,2 . Two-dimensional Fourier transform electronic spectroscopy 3-5 has mapped 6 these energy levels and their coupling in the Fenna-Matthews-Olson (FMO) bacteriochlorophyll complex, which is found in green sulphur bacteria and acts as an energy 'wire' connecting a large peripheral light-harvesting antenna, the chlorosome, to the reaction centre 7-9 . The spectroscopic data clearly document the dependence of the dominant energy transport pathways on the spatial properties of the excited-state wavefunctions of the whole bacteriochlorophyll complex 6,10 . But the intricate dynamics of quantum coherence, which has no classical analogue, was largely neglected in the analyses-even though electronic energy transfer involving oscillatory populations of donors and acceptors was first discussed more than 70 years ago 11 , and electronic quantum beats arising from quantum coherence in photosynthetic complexes have been predicted 12,13 and indirectly observed 14 . Here we extend previous twodimensional electronic spectroscopy investigations of the FMO bacteriochlorophyll complex, and obtain direct evidence for remarkably long-lived electronic quantum coherence playing an important part in energy transfer processes within this system. The quantum coherence manifests itself in characteristic, directly observable quantum beating signals among the excitons within the Chlorobium tepidum FMO complex at 77 K. This wavelike characteristic of the energy transfer within the photosynthetic complex can explain its extreme efficiency, in that it allows the complexes to sample vast areas of phase space to find the most efficient path.
Electronic coherence effects in photosynthetic light harvesting
Procedia Chemistry, 2011
Photosynthetic light harvesting is a paradigmatic example for quantum effects in biology. In this work, we review studies on quantum coherence effects in the LH2 antenna complex from purple bacteria to demonstrate how quantum mechanical rules play important roles in the speedup of excitation energy transfer, the stabilization of electronic excitations, and the robustness of light harvesting in photosynthesis. Subsequently, we present our recent theoretical studies on exciton dynamical localization and excitonic coherence generation in photosynthetic systems. We apply a variational-polaron approach to investigate decoherence of exciton states induced by dynamical fluctuations due to system-environment interactions. The results indicate that the dynamical localization of photoexcitations in photosynthetic complexes is significant and imperative for a complete understanding of coherence and excitation dynamics in photosynthesis. Moreover, we use a simple model to investigate quantum coherence effects in intercomplex excitation energy transfer in natural photosynthesis, with a focus on the likelihoods of generating excitonic coherences during the process. Our model simulations reveal that excitonic coherence between acceptor exciton states and transient nonlocal quantum correlation between distant pairs of chromophores can be generated through intercomplex energy transfer. Finally, we discuss the implications of these theoretical works and important open questions that remain to be answered.
Quantum coherence in photosynthetic complexes
2011
The initial steps of photosynthesis require the absorption and subsequent transfer of energy through an intricate network of pigment-protein complexes. Held within the protein scaffold of these complexes, chromophore molecules are densely packed and fixed in specific geometries relative to one another resulting in Coulombic coupling. Excitation energy transfer through these systems can be accomplished with near unity quantum efficiency [Wraight and Clayton, Biochim. Biophys. Acta 333, 246 (1974)]. While replication of this feat is desirable for artificial photosynthesis, the mechanism by which nature achieves this efficiency is unknown. Recent experiments have revealed the presence of long-lived quantum coherences in photosynthetic pigment-protein complexes spanning bacterial and plant species with a variety of functions and compositions. Its ubiquitous presence and wavelike energy transfer implicate quantum coherence as key to the high efficiency achieved by photosynthesis.
The Journal of Chemical Physics, 2012
Two-dimensional photon-echo experiments indicate that excitation energy transfer between chromophores near the reaction center of the photosynthetic purple bacterium Rhodobacter sphaeroides occurs coherently with decoherence times of hundreds of femtoseconds, comparable to the energy transfer time scale in these systems. The original explanation of this observation suggested that correlated fluctuations in chromophore excitation energies, driven by large scale protein motions could result in long lived coherent energy transfer dynamics. However, no significant site energy correlation has been found in recent molecular dynamics simulations of several model light harvesting systems. Instead, there is evidence of correlated fluctuations in site energy-electronic coupling and electronic coupling-electronic coupling. The roles of these different types of correlations in excitation energy transfer dynamics are not yet thoroughly understood, though the effects of site energy correlations have been well studied. In this paper, we introduce several general models that can realistically describe the effects of various types of correlated fluctuations in chromophore properties and systematically study the behavior of these models using general methods for treating dissipative quantum dynamics in complex multi-chromophore systems. The effects of correlation between site energy and inter-site electronic couplings are explored in a two state model of excitation energy transfer between the accessory bacteriochlorophyll and bacteriopheophytin in a reaction center system and we find that these types of correlated fluctuations can enhance or suppress coherence and transfer rate simultaneously. In contrast, models for correlated fluctuations in chromophore excitation energies show enhanced coherent dynamics but necessarily show decrease in excitation energy transfer rate accompanying such coherence enhancement. Finally, for a three state model of the Fenna-Matthews-Olsen light harvesting complex, we explore the influence of including correlations in inter-chromophore couplings between different chromophore dimers that share a common chromophore. We find that the relative sign of the different correlations can have profound influence on decoherence time and energy transfer rate and can provide sensitive control of relaxation in these complex quantum dynamical open systems.
Dynamic coherence in excitonic molecular complexes under various excitation conditions
Chemical Physics, 2014
We investigate the relevance of dynamic quantum coherence in the energy transfer efficiency of molecular aggregates. We contrast the dynamics after excitation of a quantum mechanical system with that of a classical system. We demonstrate how a classical description of an ensemble average can be satisfactorily interpreted either as a single system driven by a continuous force or as an ensemble of systems each driven by an impulsive force. We derive the time evolution of the density matrix for an open quantum system excited by light or by a neighboring antenna. We argue that unlike in the classical case, the quantum description does not allow for a formal decomposition of the dynamics into sudden jumps in the quantum mechanical state. Rather, there is a natural finite time-scale associated with the excitation process. We propose a simple experiment how to test the influence of this time scale on the yield of photosynthesis. Because photosynthesis is intrinsically an average process, the efficiency of photosynthesis can be assessed from the quantum mechanical expectation value calculated from the second-order response theory, which has the same validity as the perturbative description of ultrafast experiments. We demonstrate using typical parameters of the currently most studied photosynthetic antenna, the Fenna-Matthews-Olson (FMO) complex, and a typical energy transfer rate from the chlorosome baseplate, that dynamic coherences are averaged out in the complex despite excitation proceeding through a coherent superposition of its eigenstates. The dynamic coherence averages out even when the FMO model is completely free of all dissipation and dephasing. We conclude that under natural excitation conditions, coherent dynamics cannot be responsible for the remarkable efficiency of the photosynthesis, even when considering the dynamics at a single molecular level.
Coherent Vibronic Coupling in Light-Harvesting Complexes from Photosynthetic Marine Algae
The Journal of Physical Chemistry Letters, 2012
Observations of long-lived coherences in photosynthetic lightharvesting complexes utilize short pulses with broad spectral bandwidths to coherently excite multiple transitions and coherent superpositions. In order to identify the role that such quantum effects might play in efficient energy transfer, however, an alternative approach is required. We have developed a technique for two-color photon echo spectroscopy to selectively excite the pathway of interest and measure its evolution in the absence of any other excitation. We use this technique to excite a coherence pathway in phycocyanin-645 from cryptophyte algae and measure the dynamics of this coherence. A decoherence time of 500 fs was measured, and clear signatures for strong coupling between the electronic states and phonon modes were observed, allowing coherent coupling between otherwise nonresonant transitions. This provides detailed experimental evidence of the long-lived coherences and the nature of the quantum mechanical interactions between electronic states and phonon modes in phycocyanin-645 from cryptophyte marine algae. SECTION: Kinetics, Spectroscopy T he role of quantum effects in photosynthesis has been a subject of great speculation since the first observations of long-lived coherences in light-harvesting complexes. 1−4 The initial theoretical models showed that quantum coherence, by itself, actually reduces the efficiency of energy transfer, but by including some dephasing, the combination of quantum tunnelling and noise leads to highly efficient energy transfer. 5−11 Part of the reason for this enhanced transfer efficiency is that the dephasing caused by a Markovian bath of phonon modes leads to spectral broadening, which brings otherwise nonresonant transitions into resonance. Subsequent studies looked at the effect of spatial correlations of the phonon interactions 12 and non-Markovian dynamics of the system− bath interactions. 13−15 The conclusions of these studies point to a regime where the separation of the system and bath is not clear, and it is necessary to include both electronic states and vibrational modes within the description of the system. The form of the interactions between vibrational and electronic states and assumptions made about the phonon spectral density have been shown to significantly alter the calculated dynamics. Experimental details of the interactions between electronic states and the vibrational/phonon modes of the chromophores and surrounding protein matrix remain lacking. Similarly, beyond the observation of long-lived coherent coupling between exciton states, any experimental evidence for the role of quantum effects in photosynthetic energy transfer remains elusive.
Journal of Physical Chemistry B, 1998
We have employed dynamic absorption spectroscopy to monitor coherent wave packet dynamics and anisotropy decays following impulsive excitation of the B820 subunit of the LH1 light-harvesting complex, which was isolated from Rhodospirillum rubrum G9. When the lower exciton-state transition of the bacteriochlorophyll a dimer is pumped, the time-resolved pump-probe spectrum exhibits contributions from a fully Stokes shifted stimulated-emission spectrum and a nonstationary vibrational character within 40 fs of excitation. Coherent wave packet motion in both the ground state and the excited state is observed via modulations of singlewavelength transients. The photobleaching portion of the spectrum exhibits strong components only at low frequencies, 20-60 and 180 cm -1 , and a weaker component is observed at 400 cm -1 . The stimulated-emission portion of the spectrum exhibits weak modulation components at 20-60 and 180 cm -1 , but strong components are observed at fairly high frequencies: 360, 400, 470, 600, and 730 cm -1 . An anisotropy decay observed in the stimulated-emission region reports a prompt >20°tilt of the photoselected transition-dipole moment. A possible explanation for these results is that an intradimer charge-transfer event occurs on a very short time scale following optical preparation of the lower π f π* exciton state of the bacteriochlorophyll a dimer at room temperature.