Photosynthetic Energy Transfer Research Articles

Efficient quantum simulation of photosynthetic light harvesting

Near-unity energy transfer efficiency has been widely observed in natural photosynthetic complexes. This phenomenon has attracted broad interest from different fields, such as physics, biology, chemistry, and material science, as it may offer valuable insights into efficient solar-energy harvesting. Recently, quantum coherent effects have been discovered in photosynthetic light harvesting, and their potential role on energy transfer has seen the heated debate. Here, we perform an experimental quantum simulation of photosynthetic energy transfer using nuclear magnetic resonance (NMR). We show that an N-chromophore photosynthetic complex, with arbitrary structure and bath spectral density, can be effectively simulated by a system with log2N qubits. The computational cost of simulating such a system with a theoretical tool, like the hierarchical equation of motion, which is exponential in N, can be potentially reduced to requiring a just polynomial number of qubits N using NMR quantum simulation. The benefits of performing such quantum simulation in NMR are even greater when the spectral density is complex, as in natural photosynthetic complexes. These findings may shed light on quantum coherence in energy transfer and help to provide design principles for efficient artificial light harvesting.

Strongly coupled bacteriochlorin dyad studied using phase-modulated fluorescence-detected two-dimensional electronic spectroscopy.

Fluorescence-detected two-dimensional electronic spectroscopy (F-2DES) projects the third-order non-linear polarization in a system as an excited electronic state population which is incoherently detected as fluorescence. Multiple variants of F-2DES have been developed. Here, we report phase-modulated F-2DES measurements on a strongly coupled symmetric bacteriochlorin dyad, a relevant 'toy' model for photosynthetic energy and charge transfer. Coherence map analysis shows that the strongest frequency observed in the dyad is well-separated from the excited state electronic energy gap, and is consistent with a vibrational frequency readily observed in bacteriochlorin monomers. Kinetic rate maps show a picosecond relaxation timescale between the excited states of the dyad. To our knowledge this is the first demonstration of coherence and kinetic analysis using the phase-modulation approach to F-2DES.

Vibronic Wavepackets and Energy Transfer in Cryptophyte Light-Harvesting Complexes.

Determining the key features of high-efficiency photosynthetic energy transfer remains an ongoing task. Recently, there has been evidence for the role of vibronic coherence in linking donor and acceptor states to redistribute oscillator strength for enhanced energy transfer. To gain further insights into the interplay between vibronic wavepackets and energy-transfer dynamics, we systematically compare four structurally related phycobiliproteins from cryptophyte algae by broad-band pump-probe spectroscopy and extend a parametric model based on global analysis to include vibrational wavepacket characterization. The four phycobiliproteins isolated from cryptophyte algae are two "open" structures and two "closed" structures. The closed structures exhibit strong exciton coupling in the central dimer. The dominant energy-transfer pathway occurs on the subpicosecond timescale across the largest energy gap in each of the proteins, from central to peripheral chromophores. All proteins exhibit a strong 1585 cm-1 coherent oscillation whose relative amplitude, a measure of vibronic intensity borrowing from resonance between donor and acceptor states, scales with both energy-transfer rates and damping rates. Central exciton splitting may aid in bringing the vibronically linked donor and acceptor states into better resonance resulting in the observed doubled rate in the closed structures. Several excited-state vibrational wavepackets persist on timescales relevant to energy transfer, highlighting the importance of further investigation of the interplay between electronic coupling and nuclear degrees of freedom in studies on high-efficiency photosynthesis.

Identification and characterization of diverse coherences in the Fenna-Matthews-Olson complex.

The idea that excitonic (electronic) coherences are of fundamental importance to natural photosynthesis gained popularity when slowly dephasing quantum beats (QBs) were observed in the two-dimensional electronic spectra of the Fenna-Matthews-Olson (FMO) complex at 77 K. These were assigned to superpositions of excitonic states, a controversial interpretation, as the strong chromophore-environment interactions in the complex suggest fast dephasing. Although it has been pointed out that vibrational motion produces similar spectral signatures, a concrete assignment of these oscillatory signals to distinct physical processes is still lacking. Here we revisit the coherence dynamics of the FMO complex using polarization-controlled two-dimensional electronic spectroscopy, supported by theoretical modelling. We show that the long-lived QBs are exclusively vibrational in origin, whereas the dephasing of the electronic coherences is completed within 240 fs even at 77 K. We further find that specific vibrational coherences are produced via vibronically coupled excited states. The presence of such states suggests that vibronic coupling is relevant for photosynthetic energy transfer.

Photosynthetic Energy Transfer at the Quantum/Classical Border.

Quantum mechanics diverges from the classical description of our world when very small scales or very fast processes are involved. Unlike classical mechanics, quantum effects cannot be easily related to our everyday experience and are often counterintuitive to us. Nevertheless, the dimensions and time scales of the photosynthetic energy transfer processes puts them close to the quantum/classical border, bringing them into the range of measurable quantum effects. Here we review recent advances in the field and suggest that photosynthetic processes can take advantage of the sensitivity of quantum effects to the environmental 'noise' as means of tuning exciton energy transfer efficiency. If true, this design principle could be a base for 'nontrivial' coherent wave property nano-devices.

Impact of undamped and damped intramolecular vibrations on the efficiency of photosynthetic exciton energy transfer

In recent years, the role of molecular vibrations in exciton energy transfer taking place during the first stage of photosynthesis attracted increasing interest. Here, we present a model formulated as a Lindblad-type master equation that enables us to investigate the impact of undamped and especially damped intramolecular vibrational modes on the exciton energy transfer, particularly its efficiency. Our simulations confirm the already reported effects that the presence of an intramolecular vibrational mode can compensate the energy detuning of electronic states, thus promoting the energy transfer; and, moreover, that the damping of such a vibrational mode (in other words, vibrational relaxation) can further enhance the efficiency of the process by generating directionality in the energy flow. As a novel result, we show that this enhancement surpasses the one caused by pure dephasing, and we present its dependence on various system parameters (time constants of the environment-induced relaxation and excitation processes, detuning of the electronic energy levels, frequency of the intramolecular vibrational modes, Huang–Rhys factors, temperature) in dimer model systems. We demonstrate that vibrational-relaxation-enhanced exciton energy transfer (VREEET) is robust against the change of these characteristics of the system and occurs in wide ranges of the investigated parameters. With simulations performed on a heptamer model inspired by the Fenna–Matthews–Olson (FMO) complex, we show that this mechanism can be even more significant in larger systems at T = 300 K. Our results suggests that VREEET might be prevalent in light-harvesting complexes.

Non-equilibrium stationary coherences in photosynthetic energy transfer under weak-field incoherent illumination.

We present a theoretical study of the quantum dynamics of energy transfer in a model photosynthetic dimer excited by incoherent light and show that the interplay between incoherent pumping and phonon-induced relaxation, dephasing, and trapping leads to the emergence of non-equilibrium stationary states characterized by substantial stationary coherences in the energy basis. We obtain analytic expressions for these coherences in the limits of rapid dephasing of electronic excitations and of small excitonic coupling between the chromophores. The stationary coherences are maximized in the regime where the excitonic coupling is small compared to the trapping rate. We further show that the non-equilibrium coherences anti-correlate with the energy transfer efficiency in the regime of localized coupling to the reaction center and that no correlation exists under delocalized (Förster) trapping conditions.

The energy transfer dynamics in C-phycocyanin hexamer from <italic>Spirulina platensis</italic>

Photosynthesis is an ancient and important conversion of solar light to biological energy in photosynthetic organisms. Phycobilisome (PBS) system in cyanobacteria and red algae is one of two major light-harvesting systems of photosynthetic oxygen organisms. PBS is aggregation of water-soluble phycobiliproteins (PBPs) which are distinctively colored group of disk-shaped macromolecular proteins bearing covalently attached open-chain tetrapyrroles known as phycobilins. PBPs are capable to absorb solar light and transfer energy to the chlorophyll of photosynthetic reaction center with a high efficiency. Light energy absorbed by phycobilins is transmitted between the subunits, and then transmitted between different PBPs, finally to the photoreaction center located on the thylakoid membrane. The energy transfer between PBPs is very fast and high efficiency. Because energy can be transferred in different chromophores and there are a large number of chromophores in PBPs, the energy transfer path of PBPs is complex and diverse. In the past 20 years, energy transfer process of PBPs have been analyzed by time-resolved fluorescence spectroscopy because a large shift of the fluorescence peaks can be clearly observed. For example, Zhang et al. estimated the time constant for energy transfer from PC (rod) to APC (core) as 18 ps and 55 ps based on PBPs crystal structures and time-resolved fluorescence spectra of the rod-core complex. However, due to the technical bottleneck of theoretical simulation and spectral experimental detection, the research on the physical mechanism of photosynthetic energy transfer is relatively slow. In recent years, the ultrafast spectrum time resolution has been continuously improved, which provides the conditions for studying the energy transfer of PBPs. In this paper, the mechanism of energy transfer in C-phycocyanin hexamer from Spirulina platensis was studied by ultrafast time-resolved fluorescence spectroscopy. The energy transfer pathway and the related transfer parameters in the C-phycocyanin hexamer were identified by the fitting of the fluorescence decay curve at different detection wavelengths. It was proved that the energy transfer of C-phycocyanin hexamer had four time components from the experiment, which are 6, 22, 280 and 1470 ps, respectively, then the time components were identified and discussed. This study reflects the energy transfer kinetics between different chromophores in C-phycocyanin and provides important experimental data for solving the relationship between the structure and function of PBPs. At the same time, our study has important value for the understanding of the primary process of photosynthesis. In the future, if the resolution of a streak camera can be raised to femtoseconds, it is possible to find more energy transfer paths, and thus it is expected to make a breakthrough in the ultrafast and ultra-efficient energy transfer mechanism of PBPs.

Effect of Time-Delayed Feedback on the Interaction of a Dimer System with its Environment

In this work, we report modeling of non-Markovian open quantum systems, consisting of an excitonic dimer that displays memory effect due to time delayed interaction with its environment. We, indeed investigate the effect of these time delays on quantum coherence and excitation dynamical behavior in the time domain generally considered for photosynthetic experiments (few hundred femtoseconds). In particular, we show that the coherence is maintained for periods proportional to time delays. Additionally, if delay is taken into account, coupling to the environment can be tuned to lower values, unlike in previous studies. This kind of intriguing effect can, therefore, when generalized to complete systems, permit more control on the experimental parameters, which may lead to more accurate description of the photosynthetic energy transfer functioning and subsequent applications in artificial photovoltaic research.

Nature does not rely on long-lived electronic quantum coherence for photosynthetic energy transfer

During the first steps of photosynthesis, the energy of impinging solar photons is transformed into electronic excitation energy of the light-harvesting biomolecular complexes. The subsequent energy transfer to the reaction center is commonly rationalized in terms of excitons moving on a grid of biomolecular chromophores on typical timescales [Formula: see text]100 fs. Today's understanding of the energy transfer includes the fact that the excitons are delocalized over a few neighboring sites, but the role of quantum coherence is considered as irrelevant for the transfer dynamics because it typically decays within a few tens of femtoseconds. This orthodox picture of incoherent energy transfer between clusters of a few pigments sharing delocalized excitons has been challenged by ultrafast optical spectroscopy experiments with the Fenna-Matthews-Olson protein, in which interference oscillatory signals up to 1.5 ps were reported and interpreted as direct evidence of exceptionally long-lived electronic quantum coherence. Here, we show that the optical 2D photon echo spectra of this complex at ambient temperature in aqueous solution do not provide evidence of any long-lived electronic quantum coherence, but confirm the orthodox view of rapidly decaying electronic quantum coherence on a timescale of 60 fs. Our results can be considered as generic and give no hint that electronic quantum coherence plays any biofunctional role in real photoactive biomolecular complexes. Because in this structurally well-defined protein the distances between bacteriochlorophylls are comparable to those of other light-harvesting complexes, we anticipate that this finding is general and directly applies to even larger photoactive biomolecular complexes.

PyLDM - An open source package for lifetime density analysis of time-resolved spectroscopic data.

Ultrafast spectroscopy offers temporal resolution for probing processes in the femto- and picosecond regimes. This has allowed for investigation of energy and charge transfer in numerous photoactive compounds and complexes. However, analysis of the resultant data can be complicated, particularly in more complex biological systems, such as photosystems. Historically, the dual approach of global analysis and target modelling has been used to elucidate kinetic descriptions of the system, and the identity of transient species respectively. With regards to the former, the technique of lifetime density analysis (LDA) offers an appealing alternative. While global analysis approximates the data to the sum of a small number of exponential decays, typically on the order of 2-4, LDA uses a semi-continuous distribution of 100 lifetimes. This allows for the elucidation of lifetime distributions, which may be expected from investigation of complex systems with many chromophores, as opposed to averages. Furthermore, the inherent assumption of linear combinations of decays in global analysis means the technique is unable to describe dynamic motion, a process which is resolvable with LDA. The technique was introduced to the field of photosynthesis over a decade ago by the Holzwarth group. The analysis has been demonstrated to be an important tool to evaluate complex dynamics such as photosynthetic energy transfer, and complements traditional global and target analysis techniques. Although theory has been well described, no open source code has so far been available to perform lifetime density analysis. Therefore, we introduce a python (2.7) based package, PyLDM, to address this need. We furthermore provide a direct comparison of the capabilities of LDA with those of the more familiar global analysis, as well as providing a number of statistical techniques for dealing with the regularization of noisy data.

The contributions of 49ers to the measurements and models of ultrafast photosynthetic energy transfer.

Progress in measuring and understanding the mechanism of the elementary energy transfer steps in photosynthetic light harvesting from roughly 1949 to the present is sketched with a focus on the group of scientists born in 1949 ± 1. Improvements in structural knowledge, laser spectroscopic methods, and quantum dynamical theories have led to the ability to record and calculate with reasonable accuracy the timescales of elementary energy transfer steps. The significance of delocalized excited states and of near-field Coulombic coupling is noted. The microscopic understanding enables consistent coarse graining and should enable a much-improved understanding of the regulation of photosynthetic light harvesting.

Vibronic Coupling as a Design Principle to Optimize Photosynthetic Energy Transfer

In this issue of Chem , Dean et al. report on observations of vibronic enhancement to energy transfer in the cryptophyte algae light-harvesting complex PC645 by using two-dimensional electronic spectroscopy.

Role of an elliptical structure in photosynthetic energy transfer: Collaboration between quantum entanglement and thermal fluctuation.

Recent experiments have revealed that the light-harvesting complex 1 (LH1) in purple photosynthetic bacteria has an elliptical structure. Generally, symmetry lowering in a structure leads to a decrease in quantum effects (quantum coherence and entanglement), which have recently been considered to play a role in photosynthetic energy transfer, and hence, elliptical structure seems to work against efficient photosynthetic energy transfer. Here we analyse the effect of an elliptical structure on energy transfer in a purple photosynthetic bacterium and reveal that the elliptical distortion rather enhances energy transfer from peripheral LH2 to LH1 at room temperature. Numerical results show that quantum entanglement between LH1 and LH2 is formed over a wider range of high energy levels than would have been the case with circular LH1. Light energy absorbed by LH2 is thermally pumped via thermal fluctuation and is effectively transferred to LH1 through the entangled states at room temperature rather than at low temperature. This result indicates the possibility that photosynthetic systems adopt an elliptical structure to effectively utilise both quantum entanglement and thermal fluctuation at physiological temperature.

Semiclassical Path Integral Dynamics: Photosynthetic Energy Transfer with Realistic Environment Interactions.

This article reviews recent progress in the theoretical modeling of excitation energy transfer (EET) processes in natural light harvesting complexes. The iterative partial linearized density matrix path-integral propagation approach, which involves both forward and backward propagation of electronic degrees of freedom together with a linearized, short-time approximation for the nuclear degrees of freedom, provides an accurate and efficient way to model the nonadiabatic quantum dynamics at the heart of these EET processes. Combined with a recently developed chromophore-protein interaction model that incorporates both accurate ab initio descriptions of intracomplex vibrations and chromophore-protein interactions treated with atomistic detail, these simulation tools are beginning to unravel the detailed EET pathways and relaxation dynamics in light harvesting complexes.

Mutations to R. sphaeroides Reaction Center Perturb Energy Levels and Vibronic Coupling but Not Observed Energy Transfer Rates.

The bacterial reaction center is capable of both efficiently collecting and quickly transferring energy within the complex; therefore, the reaction center serves as a convenient model for both energy transfer and charge separation. To spectroscopically probe the interactions between the electronic excited states on the chromophores and their intricate relationship with vibrational motions in their environment, we examine coherences between the excited states. Here, we investigate this question by introducing a series of point mutations within 12 Å of the special pair of bacteriochlorophylls in the Rhodobacter sphaeroides reaction center. Using two-dimensional spectroscopy, we find that the time scales of energy transfer dynamics remain unperturbed by these mutations. However, within these spectra, we detect changes in the mixed vibrational-electronic coherences in these reaction centers. Our results indicate that resonance between bacteriochlorophyll vibrational modes and excitonic energy gaps promote electronic coherences and support current vibronic models of photosynthetic energy transfer.

Direct observation of multistep energy transfer in LHCII with fifth-order 3D electronic spectroscopy.

During photosynthesis, sunlight is efficiently captured by light-harvesting complexes, and the excitation energy is then funneled towards the reaction centre. These photosynthetic excitation energy transfer (EET) pathways are complex and proceed in a multistep fashion. Ultrafast two-dimensional electronic spectroscopy (2DES) is an important tool to study EET processes in photosynthetic complexes. However, the multistep EET processes can only be indirectly inferred by correlating different cross peaks from a series of 2DES spectra. Here we directly observe multistep EET processes in LHCII using ultrafast fifth-order three-dimensional electronic spectroscopy (3DES). We measure cross peaks in 3DES spectra of LHCII that directly indicate energy transfer from excitons in the chlorophyll b (Chl b) manifold to the low-energy level chlorophyll a (Chl a) via mid-level Chl a energy states. This new spectroscopic technique allows scientists to move a step towards mapping the complete complex EET processes in photosynthetic systems.

Response of growth, photosynthetic pigments, laser-induced pigment fluorescence, antioxidant enzymes and lipid peroxidation to ultraviolet-B radiation in two cyanobacteria

Cyanobacteria, Anabaena cylindrica and Synechocystis PCC 6803 grown in batch culture were used to assess the effect of UV-B radiation on growth, photosynthetic pigments, photosynthetic excitation energy transfer by laser induced fluorescence, antioxidant activities, lipid peroxidation, proline and protein content. The photosynthetic apparatus, photosynthetic pigments along with excitation energy transfer are the main targets of UV-B radiation. UV-B radiation was found to inhibit the growth, photosynthetic pigments and excitation energy transfer in both cyanobacterial species. The activities of superoxide dismutase, catalase and peroxidase were significantly increased in both Anabaena cylindrica and Synechocystis PCC 6803. Malondialdehyde content was increased more than two folds in both the cyanobacterial species under prolonged incubation with UV light. In Anabaena cylindrica protein content decreased continuously with increasing duration of UV-B radiation. On the other hand in Synechocystis PCC 6803 the protein content increased up to 48 h UV-B treatment and decreased subsequently for 60 and 72 h UV-B exposure. The results indicate that UV-B radiation causes damage in cyanobacteria at several levels.

Impact of environmentally induced fluctuations on quantum mechanically mixed electronic and vibrational pigment states in photosynthetic energy transfer and 2D electronic spectra.

Recently, nuclear vibrational contribution signatures in two-dimensional (2D) electronic spectroscopy have attracted considerable interest, in particular as regards interpretation of the oscillatory transients observed in light-harvesting complexes. These transients have dephasing times that persist for much longer than theoretically predicted electronic coherence lifetime. As a plausible explanation for this long-lived spectral beating in 2D electronic spectra, quantum-mechanically mixed electronic and vibrational states (vibronic excitons) were proposed by Christensson et al. [J. Phys. Chem. B 116, 7449 (2012)] and have since been explored. In this work, we address a dimer which produces little beating of electronic origin in the absence of vibronic contributions, and examine the impact of protein-induced fluctuations upon electronic-vibrational quantum mixtures by calculating the electronic energy transfer dynamics and 2D electronic spectra in a numerically accurate manner. It is found that, at cryogenic temperatures, the electronic-vibrational quantum mixtures are rather robust, even under the influence of the fluctuations and despite the small Huang-Rhys factors of the Franck-Condon active vibrational modes. This results in long-lasting beating behavior of vibrational origin in the 2D electronic spectra. At physiological temperatures, however, the fluctuations eradicate the mixing, and hence, the beating in the 2D spectra disappears. Further, it is demonstrated that such electronic-vibrational quantum mixtures do not necessarily play a significant role in electronic energy transfer dynamics, despite contributing to the enhancement of long-lived quantum beating in 2D electronic spectra, contrary to speculations in recent publications.

Experimental implementations of two-dimensional fourier transform electronic spectroscopy.

Two-dimensional electronic spectroscopy (2DES) reveals connections between an optical excitation at a given frequency and the signals it creates over a wide range of frequencies. These connections, manifested as cross-peak locations and their lineshapes, reflect the underlying electronic and vibrational structure of the system under study. How these spectroscopic signatures evolve in time reveals the system dynamics and provides a detailed picture of coherent and incoherent processes. 2DES is rapidly maturing and has already found numerous applications, including studies of photosynthetic energy transfer and photochemical reactions and many-body interactions in nanostructured materials. Many systems of interest contain electronic transitions spanning the ultraviolet to the near infrared and beyond. Most 2DES measurements to date have explored a relatively small frequency range. We discuss the challenges of implementing 2DES and compare and contrast different approaches in terms of their information content, ease of implementation, and potential for broadband measurements.