Photosynthetic Energy Transfer Research Articles

Probing the design principles of photosynthetic systems through fluorescence noise measurement

Elucidating the energetic processes which govern photosynthesis, the engine of life on earth, are an essential goal both for fundamental research and for cutting-edge biotechnological applications. Fluorescent signal of photosynthetic markers has long been utilised in this endeavour. In this research we demonstrate the use of fluorescent noise analysis to reveal further layers of intricacy in photosynthetic energy transfer. While noise is a common tool analysing dynamics in physics and engineering, its application in biology has thus far been limited. Here, a distinct behaviour in photosynthetic pigments across various chemical and biological environments is measured. These changes seem to elucidate quantum effects governing the generation of oxidative radicals. Although our method offers insights, it is important to note that the interpretation should be further validated expertly to support as conclusive theory. This innovative method is simple, non-invasive, and immediate, making it a promising tool to uncover further, more complex energetic events in photosynthesis, with potential uses in environmental monitoring, agriculture, and food-tech.

Simulation of a spin-boson model by iterative optimization of a parametrized quantum circuit

Time evolution of the populations of spin states coupled with bosons, which can be a model of photosynthetic excitation energy transfer of dye molecules surrounded by proteins, is simulated using the projected-variational quantum dynamics algorithm. By a transformation of the Hamiltonian describing the spin-boson model into the one-dimensional nearest-neighbor form, it is shown that the spin-boson model can be simulated using the sequential ansatz even if a quantum computer has limited connectivity. The optimization of the parametrized quantum circuits is performed by the gradient descent method on a classical computer using the automatic differentiation, and the population of the spins is simulated on a noisy intermediate-scale quantum computer. The error originating from the quantum computing is mitigated by the Clifford data regression, in which the noise channel is estimated using the data obtained from all the time steps.

Manipulation of photosynthetic energy transfer by vibrational strong coupling.

Uncovering the mystery of efficient and directional energy transfer in photosynthetic organisms remains a critical challenge in quantum biology. Recent experimental evidence and quantum theory developments indicate the significance of quantum features of molecular vibrations in assisting photosynthetic energy transfer, which provides the possibility of manipulating the process by controlling molecular vibrations. Here, we propose and theoretically demonstrate efficient manipulation of photosynthetic energy transfer by using vibrational strong coupling between the vibrational state of a Fenna-Matthews-Olson (FMO) complex and the vacuum state of an optical cavity. Specifically, based on a full-quantum analytical model to describe the strong coupling effect between the optical cavity and molecular vibration, we realize efficient manipulation of energy transfer efficiency (from 58% to 92%) and energy transfer time (from 20 to 500ps) in one branch of FMO complex by actively controlling the coupling strength and the quality factor of the optical cavity under both near-resonant and off-resonant conditions, respectively. Our work provides a practical scenario to manipulate photosynthetic energy transfer by externally interfering molecular vibrations via an optical cavity and a comprehensible conceptual framework for researching other similar systems.

Optical Non‐Reciprocity in Coupled Resonators by Detailed Balance

AbstractInspired by the photosynthetic energy transfer process, a method to realize non‐reciprocal optical transmission in an array of coupled resonators is theoretically proposed. The optical non‐reciprocity of the coupled resonators arises from the frequency gradient between adjacent cavities and the interaction with the environment, which is similar to photosynthetic energy transfer. An increase in the frequency gradient or the number of the cavities can lead to better non‐reciprocity. However, although a higher environment temperature will increase the total photon number in the coupled cavities, non‐reciprocity will be weakened. All these findings can be well described by the detailed balance. The similarity between the noise‐induced optical non‐reciprocity and exciton energy transfer in natural photosynthesis is revealed by the discovery.

Protein-Based Model for Energy Transfer between Photosynthetic Light-Harvesting Complexes Is Constructed Using a Direct Protein-Protein Conjugation Strategy.

Photosynthetic organisms utilize dynamic and complex networks of pigments bound within light-harvesting complexes to transfer solar energy from antenna complexes to reaction centers. Understanding the principles underlying the efficiency of these energy transfer processes, and how they may be incorporated into artificial light-harvesting systems, is facilitated by the construction of easily tunable model systems. We describe a protein-based model to mimic directional energy transfer between light-harvesting complexes using a circular permutant of the tobacco mosaic virus coat protein (cpTMV), which self-assembles into a 34-monomer hollow disk. Two populations of cpTMV assemblies, one labeled with donor chromophores and another labeled with acceptor chromophores, were coupled using a direct protein-protein bioconjugation method. Using potassium ferricyanide as an oxidant, assemblies containing o-aminotyrosine were activated toward the addition of assemblies containing p-aminophenylalanine. Both of these noncanonical amino acids were introduced into the cpTMV monomers through amber codon suppression. This coupling strategy has the advantages of directly, irreversibly, and site-selectively coupling donor with acceptor protein assemblies and avoids cross-reactivity with native amino acids and undesired donor-donor or acceptor-acceptor combinations. The coupled donor-acceptor model was shown to transfer energy from an antenna disk containing donor chromophores to a downstream disk containing acceptor chromophores. This model ultimately provides a controllable and modifiable platform for understanding photosynthetic interassembly energy transfer and may lead to the design of more efficient functional light-harvesting materials.

Ultrafast Dynamics of Photosynthetic Light Harvesting: Strategies for Acclimation Across Organisms.

Photosynthetic light harvesting exhibits near-unity quantum efficiency. The high efficiency is achieved through a series of energy and charge transfer steps within a network of pigment-containing proteins. Remarkably, high efficiency is conserved across many organisms despite differences in the protein structures and organization that allow each organism to respond to its own biological niche and the stressors within. In this review, we highlight recent progress toward understanding how organisms maintain optimal light-harvesting ability by acclimating to their environment. First, we review the building blocks of photosynthetic light harvesting, energy transfer, and time-resolved spectroscopic techniques. Then, we explore how three classes of photosynthetic organisms-purple bacteria, cyanobacteria, and green plants-optimize their light-harvesting apparatuses to their particular environment. Overall, research has shown that photosynthetic energy transfer is robust to changing environmental conditions, with each organism utilizing its own strategies to optimize photon capture in its particular biological niche. Expected final online publication date for the Annual Review of Physical Chemistry, Volume 74 is April 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Response of Pea Plants (Pisum sativum cv. Ran 1) to NaCl Treatment in Regard to Membrane Stability and Photosynthetic Activity.

Salinity is one of the most extreme abiotic stress factors that negatively affect the development and productivity of plants. The salt-induced injuries depend on the salt tolerance of the plant species, salt concentration, time of exposure and developmental stage. Here, we report on the response of pea plants (Pisum sativum L. cv Ran 1) to exposure to increasing salt concentrations (100, 150 and 200 mM NaCl) for a short time period (5 days) and the ability of the plants to recover after the removal of salt. The water content, membrane integrity, lipid peroxidation, pigment content and net photosynthetic rate were determined for the pea leaves of the control, treated and recovered plants. Salt-induced alterations in the primary photosynthetic reactions and energy transfer between the main pigment-protein complexes in isolated thylakoid membranes were evaluated. The pea plants were able to recover from the treatment with 100 mM NaCl, while at higher concentrations, concentration-dependent water loss, the disturbance of the membrane integrity, lipid peroxidation and an increase in the pigment content were detected. The net photosynthetic rate, electron transport through the reaction centers of PSII and PSII, activity of PSIIα centers and energy transfer between the pigment-protein complexes were negatively affected and were not restored after the removal of NaCl.

Role of Spatially Correlated Fluctuations in Photosynthetic Excitation Energy Transfer with an Equilibrium and a Nonequilibrium Initial Bath.

The transfer of excitation energy in photosynthetic light-harvesting complexes has inspired growing interest for its scientific and engineering significance. Recent experimental findings have suggested that spatially correlated environmental fluctuations may account for the existence of long-lived quantum coherent energy transfer observed even at physiological temperature. In this paper, we investigate the effects of spatial correlations on the excitation energy transfer dynamics by including a nonequilibrium initial bath in a simulated donor-acceptor model. The initial bath state, which is assumed to be either equilibrium or nonequilibrium, is expanded in powers of coupling strength within the polaron formalism of a quantum master equation. The spatial correlations of bath fluctuations strongly influence the decay of coherence in the dynamics. The role of a nonequilibrium initial bath is also influenced by spatial correlations and becomes the most conspicuous for certain degrees of spatial correlations from which we propose a picture that the spatial correlations of bath fluctuations open up new energy transfer pathways, playing a role of protecting coherence. Besides, we apply the polaron master equation approach to study the dynamics in a two-site subsystem of the FMO complex and provide a practical example that shows the versatility of this approach.

Insights into Photosynthetic Energy Transfer Gained from Free-Energy Structure: Coherent Transport, Incoherent Hopping, and Vibrational Assistance Revisited.

Giant strides in ultrashort laser pulse technology have enabled real-time observation of dynamical processes in complex molecular systems. Specifically, the discovery of oscillatory transients in the two-dimensional electronic spectra of photosynthetic systems stimulated a number of theoretical investigations exploring the possible physical mechanisms of the remarkable quantum efficiency of light harvesting processes. In this work, we revisit the elementary aspects of environment-induced fluctuations in the involved electronic energies and present a simple way to understand energy flow with the intuitive picture of relaxation in a funnel-type free-energy landscape. The presented free-energy description of energy transfer reveals that typical photosynthetic systems operate in an almost barrierless regime. The approach also provides insights into the distinction between coherent and incoherent energy transfer and the criteria by which the necessity of the vibrational assistance is considered.

Convolutional Neural Networks for Long Time Dissipative Quantum Dynamics.

Exact numerical simulations of dynamics of open quantum systems often require immense computational resources. We demonstrate that a deep artificial neural network composed of convolutional layers is a powerful tool for predicting long-time dynamics of open quantum systems provided the preceding short-time evolution of a system is known. The neural network model developed in this work simulates long-time dynamics efficiently and accurately across different dynamical regimes from weakly damped coherent motion to incoherent relaxation. The model was trained on a data set relevant to photosynthetic excitation energy transfer and can be deployed to study long-lasting quantum coherence phenomena observed in light-harvesting complexes. Furthermore, our model performs well for the initial conditions different than those used in the training. Our approach reduces the required computational resources for long-time simulations and holds the promise for becoming a valuable tool in the study of open quantum systems.

Engineering couplings for exciton transport using synthetic DNA scaffolds

Summary Control over excitons enables electronic energy to be harnessed and transported for light harvesting and molecular electronics. Such control requires nanoscale precision over the molecular components. Natural light-harvesting systems achieve this precision through sophisticated protein machinery, which is challenging to replicate synthetically. Here, we introduce a DNA-based platform that spatially organizes cyanine chromophores to construct tunable excitonic systems. We synthesized DNA-chromophore nanostructures and characterized them with ensemble ultrafast and single-molecule spectroscopy and structure-based modeling. This synthetic approach facilitated independent control over the coupling among the chromophores and between the chromophores and the environment. We demonstrated that the coupling between the chromophores and the environment could enhance exciton transport efficiency, highlighting the key role of the environment in driving exciton dynamics. Control over excitons, as reported here, offers a path toward the development of designer nanophotonic devices.

Anaerobic energy dissipation by glycosylated carotenoids in the green sulfur bacterium Chlorobaculum tepidum

Carotenoids are linear polyenes and universal pigment molecules that support natural photosynthesis by light harvesting and photoprotection. Some carotenoids are glycosylated at the end of their polyene backbone, which does not clearly affect their photochemical and optical properties. In green sulfur bacteria (GSBs), which are obligate photosynthetic anaerobes, carotenoid glycosides are specifically bound to the photosynthetic reaction center (RC) complex. The other non-glycosylated carotenoids with the same polyene backbone are located in the chlorosome, which is an extra-large light-harvesting organelle. The current study isolated a mutant strain, ΔcruC, that lacks the gene responsible for carotenoid glycosylation in the model GSB species Chlorobaculum tepidum. We examined the effects of the mutation on photosynthetic growth and energy transfer reactions. The ΔcruC mutant cells grew significantly slower than the wild-type (WT) cells under high light conditions. Energy transfer reactions were delayed between bacteriochlorophyll (BChl) a of the RC complex, despite no obvious effect observed on the organization of photosynthetic apparatuses. Kinetic analyses revealed that almost half of the excitation energy of BChl a was constitutively quenched in the WT RC complex, even under a strictly anaerobic environment. The ΔcruC mutant strain phenotype clearly indicates that glycosylated carotenoids serve as energy dissipating, not light harvesting, pigments in C. tepidum. The current understanding of natural photosynthesis is that any energy dissipation mechanisms should be to avoid generation of reactive oxygen species, which are sensitized by the triplet-excited state of chlorophylls. However, these results indicate that carotenoid glycosides found in GSB may also serve a previously unidentified function for anaerobic energy dissipation.

Influence of Quantum Feedback Control on Excitation Energy Transfer**Supported by the National Natural Science Foundation of China (Grant Nos. 11904071 and 11374085), the Key Program of the Education Department of Anhui Province (Grant Nos. KJ2017A922, KJ2019A0725, and KJ2018A0486), the Anhui Provincial Natural Science Foundation (Grant Nos. 1908085QA40, 1708085MA12, and 1708085MA10), and the Discipline Top-Notch Talents Foundation of Anhui Provincial Universities

Excitation energy transfer (EET) plays a vital role in many areas of physics and biology processes. Here we address the role of quantum-jump-based feedback control in the efficiency of EET through a chain model. Usually, the decoherence caused by dissipative noise is detrimental to the transfer efficiency. We demonstrate that feedback control can always enhance the efficiency of EET and the dependence of different feedback controls is also discussed in detail. In addition, we investigate the strategy to enhance the efficiency of EET in the Fenna–Matthews–Olson complex as a prototype for larger photosynthetic energy transfer systems.

Quantum biology revisited.

Photosynthesis is a highly optimized process from which valuable lessons can be learned about the operating principles in nature. Its primary steps involve energy transport operating near theoretical quantum limits in efficiency. Recently, extensive research was motivated by the hypothesis that nature used quantum coherences to direct energy transfer. This body of work, a cornerstone for the field of quantum biology, rests on the interpretation of small-amplitude oscillations in two-dimensional electronic spectra of photosynthetic complexes. This Review discusses recent work reexamining these claims and demonstrates that interexciton coherences are too short lived to have any functional significance in photosynthetic energy transfer. Instead, the observed long-lived coherences originate from impulsively excited vibrations, generally observed in femtosecond spectroscopy. These efforts, collectively, lead to a more detailed understanding of the quantum aspects of dissipation. Nature, rather than trying to avoid dissipation, exploits it via engineering of exciton-bath interaction to create efficient energy flow.

DNA scaffold supports long-lived vibronic coherence in an indodicarbocyanine (Cy5) dimer.

Vibronic coupling between pigment molecules is believed to prolong coherences in photosynthetic pigment–protein complexes. Reproducing long-lived coherences using vibronically coupled chromophores in synthetic DNA constructs presents a biomimetic route to efficient artificial light harvesting. Here, we present two-dimensional (2D) electronic spectra of one monomeric Cy5 construct and two dimeric Cy5 constructs (0 bp and 1 bp between dyes) on a DNA scaffold and perform beating frequency analysis to interpret observed coherences. Power spectra of quantum beating signals of the dimers reveal high frequency oscillations that correspond to coherences between vibronic exciton states. Beating frequency maps confirm that these oscillations, 1270 cm−1 and 1545 cm−1 for the 0-bp dimer and 1100 cm−1 for the 1-bp dimer, are coherences between vibronic exciton states and that these coherences persist for ∼300 fs. Our observations are well described by a vibronic exciton model, which predicts the excitonic coupling strength in the dimers and the resulting molecular exciton states. The energy spacing between those states closely corresponds to the observed beat frequencies. MD simulations indicate that the dyes in our constructs lie largely internal to the DNA base stacking region, similar to the native design of biological light harvesting complexes. Observed coherences persist on the timescale of photosynthetic energy transfer yielding further parallels to observed biological coherences, establishing DNA as an attractive scaffold for synthetic light harvesting applications.

Advances and opportunities in ultrafast X-ray crystallography and ultrafast structural optical crystallography of nuclear and electronic protein dynamics.

Both nuclear and electronic dynamics contribute to protein function and need multiple and complementary techniques to reveal their ultrafast structural dynamics response. Real-space information obtained from the measurement of electron density dynamics by X-ray crystallography provides aspects of both, while the molecular physics of coherence parameters and frequency-frequency correlation needs spectroscopy methods. Ultrafast pump-probe applications of protein dynamics in crystals provide real-space information through direct X-ray crystallographic structure analysis or through structural optical crystallographic analysis. A discussion of methods of analysis using ultrafast macromolecular X-ray crystallography and ultrafast nonlinear structural optical crystallography is presented. The current and future high repetition rate capabilities provided by X-ray free electron lasers for ultrafast diffraction studies provide opportunities for optical control and optical selection of nuclear coherence which may develop to access higher frequency dynamics through improvements of sensitivity and time resolution to reveal coherence directly. Specific selection of electronic coherence requires optical probes, which can provide real-space structural information through photoselection of oriented samples and specifically in birefringent crystals. Ultrafast structural optical crystallography of photosynthetic energy transfer has been demonstrated, and the theory of two-dimensional structural optical crystallography has shown a method for accessing the structural selection of electronic coherence.

Effect of Plasmon Stimulation on the Extraction of Photosynthetic Electrons from Thylakoid Membranes

Because of extremely high internal quantum efficiency of photosynthesis, photosynthetic bio-solar energy conversion has drawn much attention recently in the field of renewable energy. Thylakoid membranes (TMs) are the place where photosynthesis occurs. Since TMs can be easily isolated from plants or algae and remain stable after isolation, they are widely used in photosynthetic energy transfer systems. However, despite its high conversion efficiency from photons to photosynthetic electron (PE), their overall efficiency is limited due to limited absorption of incident photons and low extraction efficiency of PEs. Therefore, several approaches were developed to increase PE extraction by improving electrical connections between TMs and electrodes such as amine or carboxyl modified carbon nanotube electrode, titanium oxide (TiO2) modified electrode or reduced graphene oxide (rGO) modified electrode. Furthermore, PE extraction can also be increased by stimulating photosynthesis to produce more PEs. Recently, it was demonstrated that photosynthesis stimulation could be achieved by inducing localized plasmon field very close to the light energy harvesting complexes within isolated photosystem I or II. In this study, we aimed to enhance PE extraction by stimulating photosynthesis using plasmon induced resonance energy transfer (PIRET). Gold nanorod (AuNR) was used to induce plasmonic field close to the TMs for photosynthesis stimulation and the geometry of AuNR was carefully selected to match its plasmon resonance wavelength with the absorption wavelengths of photosystem I or II within TMs. Therefore, AuNRs of 17 nm width and 45 nm length were chosen to have their plasmon resonance peak at 675 nm. On the other hand, since plasmonic energy can be transferred only in a few nanometer ranges, AuNR should be located very close to TM. Therefore, a tethering molecule which can link AuNR and TM was added to attach the AuNRs to TMs. The tethering molecule has poly ethylene glycol (PEG) chain and two functional groups of thiol group (-SH) and succinimide ester (NHS ester) group at each terminal end. To make AuNR-PEG-TM conjugation, the tethering molecule solution was added to an AuNR in distilled water (DIW) suspension to form AuNR-PEG-NHS. Then, a TM solution with phosphate buffer saline (PBS) was added to the mixture so that AuNR-PEG-TM conjugation was finally formed. Each intermediate product was characterized using SEM, TEM, optical, fluorescence spectroscopy, and XPS analysis. The PE currents from AuNR-PEG-TM was measured and compared to PE currents from pure TM. With the AuNR-PEG-TM conjugation, the PE current was increased by 400% compared to the PE currents of pure TM.

Lack of long-lived quantum coherence in the photosynthetic energy transfer

We have studied the FMO, LHCII and PSII reaction center complex by electronic 2D spectroscopy. At ambient temperature the electronic coherences are too short lived to play any functional role in the natural energy transfer.

Two-dimensional electronic vibrational spectroscopy and ultrafast excitonic and vibronic photosynthetic energy transfer.

Two-dimensional electronic-vibrational (2DEV) spectroscopy is a new coherent spectroscopic technique, which shows considerable promise for unravelling complex molecular dynamics. In this Discussion we describe an application to the energy transfer pathway in the major light harvesting protein, LHCII, providing new data on the center line slopes (CLS) of the spectral peaks. The CLS provides information that appears unique to the 2DEV method. We then outline a general approach to calculating 2DEV spectra which is valid for strongly and weakly coupled molecular systems. We conclude with some prospects for the future development of 2DEV spectroscopy and its theoretical analysis.

Quantum coherence in ultrafast photo-driven charge separation.

Coherent interactions are prevalent in photodriven processes, ranging from photosynthetic energy transfer to superexchange-mediated electron transfer, resulting in numerous studies aimed towards identifying and understanding these interactions. A key motivator of this interest is the non-statistical scaling laws that result from coherently traversing multiple pathways due to quantum interference. To that end, we employed ultrafast transient absorption spectroscopy to measure electron transfer in two donor-acceptor molecular systems comprising a p-(9-anthryl)-N,N-dimethylaniline chromophore/electron donor and either one or two equivalent naphthalene-1,8:4,5-bis(dicarboximide) electron acceptors at both ambient and cryogenic temperatures. The two-acceptor compound shows a statistical factor of 2.1 ± 0.2 rate enhancement at room temperature and a non-statistical factor of 2.6 ± 0.2 rate enhancement at cryogenic temperatures, suggesting correlated interactions between the two acceptors with the donor and with the bath modes. Comparing the charge recombination rates indicates that the electron is delocalized over both acceptors at low temperature but localized on a single acceptor at room temperature. These results highlight the importance of shielding the system from bath fluctuations to preserve and ultimately exploit the coherent interactions.