Electronic coherence effects in photosynthetic light harvesting

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.     

Two-dimensional electronic spectroscopy reveals ultrafast energy diffusion in chlorosomes

Chlorosomes are light-harvesting antennae that enable exceptionally efficient light energy capture and excitation transfer. They are found in certain photosynthetic bacteria, some of which live in extremely low-light environments. In this work, chlorosomes from the green sulfur bacterium Chlorobaculum tepidum were studied by coherent electronic two-dimensional (2D) spectroscopy. Previously uncharacterized ultrafast energy transfer dynamics were followed, appearing as evolution of the 2D spectral line-shape during the first 200 fs after excitation. Observed initial energy flow through the chlorosome is well explained by effective exciton diffusion on a sub-100 fs time scale, which assures efficiency and robustness of the process. The ultrafast incoherent diffusion-like behavior of the excitons points to a disordered energy landscape in the chlorosome, which leads to a rapid loss of excitonic coherences between its structural subunits. This disorder prevents observation of excitonic coherences in the experimental data and implies that the chlorosome as a whole does not function as a coherent light-harvester.     

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.

Dyes coupled to DNA display distance-dependent vibronic couplings that prolongs quantum coherences detected with 2D spectroscopy.     

Modeling of photosynthetic light-harvesting: From structure to function

In order to bridge the gap between the crystal structure of photosynthetic pigment-protein complexes and the data gathered in optical experiments, two essential problems need to be solved. On one hand, theories of optical spectra and excitation energy transfer have to be developed that take into account the pigment-pigment (excitonic) and the pigment-protein (exciton-vibrational) coupling on an equal footing. On the other hand, the parameters entering these theories need to be calculated from the structural data. Good agreement between simulations and experimental data then allows to draw conclusions on structure-function relationships of these complexes and to make predictions. In the development of theory, a delicate question is how to describe the interplay between the quantum dynamics of excitons and the dephasing of coherences by the coupling of excitons to protein vibrations. Quantum mechanic coherences are utilized for efficient light harvesting. In the reaction centers of purple bacteria an energy sink is created by a coherent coupling of exciton states to intermolecular charge transfer states. The dephasing of coherences can be monitored, e.g., by the temperature dependent shift of optical lines. In the Fenna-Matthews-Olson protein, which acts as an excitation energy wire between the outer chlorosome antenna and the reaction center complex, an energy funnel for efficient light-harvesting is formed by the pigment-protein coupling. The protein shifts the local transition energies of the pigments, the so-called site energies in a specific way, such that pigments facing the reaction center are redshifted with respect to those on the chlorosome side. In the light-harvesting complex of higher plants an excitation energy funnel is created by the use of two different types of chlorophyll (Chl) pigments, Chla and Chlb and by the pigment-protein coupling that creates an energy sink at Chla 610 located in the stromal layer at the periphery of the complex. The close contact between Chla and Chlb gives rise to ultrafast subpicosecond exciton transfer, whereas dynamic localization effects are inferred to lead to long ps relaxation times between the majority of Chla pigments.     

Two-dimensional spectroscopy can distinguish between decoherence and dephasing of zero-quantum coherences

Recent experiments on a variety of photosynthetic antenna systems have revealed that coherences among electronic states persist longer than previously anticipated. In an ensemble measurement, the observed dephasing of a coherent state can occur because of either disorder across the ensemble or decoherence from interactions with the bath. Distinguishing how much such disorder affects the experimentally observed dephasing rate is paramount for understanding the role that quantum coherence may play in energy transfer through these complexes. Here, we show that two-dimensional electronic spectra can distinguish between the limiting cases of homogeneous dephasing (decoherence) and inhomogeneous dephasing by examining how the quantum beat frequency changes within a cross peak. For the antenna complex LH2 isolated from Rhodobacter sphaeroides , we find that dephasing of the coherence between the B850 and B800 rings arises predominantly from inhomogeneity. In contrast, within the Fenna-Matthews-Olson (FMO) complex from Chlorobium tepidum , dephasing of the coherence between the first two excitons appears quite homogeneous. Thus, the observed dephasing rate sets an upper bound on decoherence for the LH2 complex while establishing both an upper and lower bound for the FMO complex.     

Geometry Effects on Light‐Harvesting Complex's Light Absorption and Energy Transfer in Purple Bacteria

Light‐harvesting complexes (LHC) in photosynthetic organisms perform the major function of light absorption and energy transportation. Optical spectrum of LHC provides a detailed understanding of the molecular mechanisms involved in the excitation energy transfer (EET) processes, which has been widely studied. Here, we study how the geometric property of LHC in Rhodospirillum (Rs.) molischianum would affect its spectral characteristics and energy transfer process. By adopting the effective Hamiltonian and the dipole–dipole approximation, we calculate the exciton level structures for the LH2 ring and LH1 ring and the energy transfer time between different LHCs under various structural parameters and different rotational symmetries. Our numerical results show that the LHC's absorption peaks and the energy transfer time between different LHCs can be modified by changing the geometric configurations. Our study may be beneficial to the applications in designing highly efficient photovoltaic cell and other artificial photosynthetic systems.     

Characterization and quantification of the role of coherence in ultrafast quantum biological experiments using quantum master equations,atomistic simulations,and quantum process tomography

Long-lived electronic coherences in various photosynthetic complexes at cryogenic and room temperature have generated vigorous efforts both in theory and experiment to understand their origins and explore their potential role to biological function. The ultrafast signals resulting from the experiments that show evidence for these coherences result from many contributions to the molecular polarization. Quantum process tomography (QPT) is a technique whose goal is that of obtaining the time-evolution of all the density matrix elements based on a designed set of experiments with different preparation and measurements. The QPT procedure was conceived in the context of quantum information processing to characterize and understand general quantum evolution of controllable quantum systems, for example while carrying out quantum computational tasks. We introduce our QPT method for ultrafast experiments, and as an illustrative example, apply it to a simulation of a two-chromophore subsystem of the Fenna-Matthews-Olson photosynthetic complex, which was recently shown to have long-lived quantum coherences. Our Fenna-Matthews-Olson model is constructed using an atomistic approach to extract relevant parameters for the simulation of photosynthetic complexes that consists of a quantum mechanics/molecular mechanics approach combined with molecular dynamics and the use of state-of-the-art quantum master equations. We provide a set of methods that allow for quantifying the role of quantum coherence, dephasing, relaxation and other elementary processes in energy transfer efficiency in photosynthetic complexes, based on the information obtained from the atomistic simulations, or, using QPT, directly from the experiment. The ultimate goal of the combination of this diverse set of methodologies is to provide a reliable way of quantifying the role of long-lived quantum coherences and obtain atomistic insight of their causes.     

Quantitative investigations of quantum coherence for a light-harvesting protein at conditions simulating photosynthesis

Recent measurements using two-dimensional electronic spectroscopy (2D ES) have shown that the initial dynamic response of photosynthetic proteins can involve quantum coherence. We show how electronic coherence can be differentiated from vibrational coherence in 2D ES. On that basis we conclude that both electronic and vibrational coherences are observed in the phycobiliprotein light-harvesting complex PC645 from Chroomonas sp. CCMP270 at ambient temperature. These light-harvesting antenna proteins of the cryptophyte algae are suspended in the lumen, where the pH drops significantly under sustained illumination by sunlight. Here we measured 2D ES of PC645 at increasing levels of acidity to determine if the change in pH affects the quantum coherence; quantitative analysis reveals that the dynamics are insensitive to the pH change.     

Signatures of correlated excitonic dynamics in two-dimensional spectroscopy of the Fenna-Matthew-Olson photosynthetic complex

Long-lived excitonic coherence in photosynthetic proteins has become an exciting area of research because it may provide design principles for enhancing the efficiency of energy transfer in a broad range of materials. In this publication, we provide new evidence that long-lived excitonic coherence in the Fenna-Mathew-Olson pigment-protein (FMO) complex is consistent with the assumption of cross correlation in the site basis, indicating that each site shares bath fluctuations. We analyze the structure and character of the beating crosspeak between the two lowest energy excitons in two-dimensional (2D) electronic spectra of the FMO Complex. To isolate this dynamic signature, we use the two-dimensional linear prediction Z-transform as a platform for filtering coherent beating signatures within 2D spectra. By separating signals into components in frequency and decay rate representations, we are able to improve resolution and isolate specific coherences. This strategy permits analysis of the shape, position, character, and phase of these features. Simulations of the crosspeak between excitons 1 and 2 in FMO under different regimes of cross correlation verify that statistically independent site fluctuations do not account for the elongation and persistence of the dynamic crosspeak. To reproduce the experimental results, we invoke near complete correlation in the fluctuations experienced by the sites associated with excitons 1 and 2. This model contradicts ab initio quantum mechanic∕molecular mechanics simulations that observe no correlation between the energies of individual sites. This contradiction suggests that a new physical model for long-lived coherence may be necessary. The data presented here details experimental results that must be reproduced for a physical model of quantum coherence in photosynthetic energy transfer.     

ENERGY TRANSFER VIA PROTEIN-PROTEIN INTERACTION IN RENILLA BIOLUMINESCENCE

Abstract—Radiationless energy transfer is known to play biologically important roles in both photosynthesis and bioluminescence. In photosynthesis, accessory pigments serve as "antennae", transferring excitation energy into the "reaction centers". In the bioluminescent coelenterates, energy is transferred from the site of reaction via an accessory protein known as the green-fluorescent protein (GFP). Coelenterate bioluminescence systems such as that of the sea pansy, Renilla , are well characterized biochemically, and their energy transfer process can be duplicated in vitro using isolated and purified components. We have measured efficient in vitro energy transfer from the electronic excited state of the enzyme-bound oxyluciferin to the green-fluorescent protein at protein concentrations of 0.1 μ M . We have also demonstrated a 1:l complex between these proteins, under conditions of energy transfer, by the chromato-graphic technique of Hummel and Dreyer. These observations indicate that bioluminescent energy transfer is mediated via protein-protein interaction. Furthermore, with inter-species cross-reaction studies and protein modification techniques we have shown that the interaction between luciferase and GFP is highly specific. These features make the Renilla system an attractive alternative to the photosynthetic systems as a tool for studying radiationless energy transfer.     

A photosynthetic biosensor with enhanced electron transfer generation realized by laser printing technology

One of the limits of current electrochemical biosensors is a lack of methods providing stable and highly efficient junctions between biomaterial and solid-state devices. This paper shows how laser-induced forward transfer (LIFT) can enable efficient electron transfer from photosynthetic biomaterial immobilized on screen-printed electrodes (SPE). The ideal pattern, in terms of photocurrent signal of thylakoid droplets giving a stable response signal with a current intensity of approximately 335 ± 13 nA for a thylakoid mass of 28 ± 4 ng, was selected. It is shown that the efficiency of energy production of a photosynthetic system can be strongly enhanced by the LIFT process, as demonstrated by use of the technique to construct an efficient and sensitive photosynthesis-based biosensor for detecting herbicides at nanomolar concentrations.     

Energy transfer between surface-immobilized light-harvesting chlorophyll a/b complex (LHCII) studied by surface plasmon field-enhanced fluorescence spectroscopy (SPFS)

The major light-harvesting chlorophyll a/b complex (LHCII) of the photosynthetic apparatus in green plants can be viewed as a protein scaffold binding and positioning a large number of pigment molecules that combines rapid and efficient excitation energy transfer with effective protection of its pigments from photobleaching. These properties make LHCII potentially interesting as a light harvester (or a model thereof) in photoelectronic applications. Most of such applications would require the LHCII to be immobilized on a solid surface. In a previous study we showed the immobilization of recombinant LHCII on functionalized gold surfaces via a 6-histidine tag (His tag) in the protein moiety. In this work the occurrence and efficiency of Fo?rster energy transfer between immobilized LHCII on a functionalized surface have been analyzed by surface plasmon field-enhanced fluorescence spectroscopy (SPFS). A near-infrared dye was attached to some but not all of the LHC complexes, serving as an energy acceptor to chlorophylls. Analysis of the energy transfer from chlorophylls to this acceptor dye yielded information about the extent of intercomplex energy transfer between immobilized LHCII.     

Influence of environment induced correlated fluctuations in electronic coupling on coherent excitation energy transfer dynamics in model photosynthetic systems

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.     

Artificial light-harvesting arrays: electronic energy migration and trapping on a sphere and between spheres

A sophisticated model of the natural light-harvesting antenna has been devised by decorating a C(60) hexa-adduct with ten yellow and two blue boron dipyrromethene (Bodipy) dyes in such a way that the dyes retain their individuality and assist solubility of the fullerene. Unusually, the fullerene core is a poor electron acceptor and does not enter into light-induced electron-transfer reactions with the appended dyes, but ineffective electronic energy transfer from the excited-state dye to the C(60) residue competes with fluorescence from the yellow dye. Intraparticle electronic energy transfer from yellow to blue dyes can be followed by steady-state and time-resolved fluorescence spectroscopy and by excitation spectra for isolated C(60) nanoparticles dissolved in dioxane at 293 K and at 77 K. The decorated particles can be loaded into polymer films by spin coating from solution. In the dried film, efficient energy transfer occurs such that photons absorbed by the yellow dye are emitted by the blue dye. Films can also be prepared to contain C(60) nanoparticles loaded with the yellow Bodipy dye but lacking the blue dye and, under these circumstances, electronic energy migration occurs between yellow dyes appended to the same nanoparticle and, at higher loading, to dye molecules on nearby particles. Doping these latter polymer films with the mixed-dye nanoparticle coalesces these multifarious processes in a single system. Thus, long-range energy migration occurs among yellow dyes attached to different particles before trapping at a blue dye. In this respect, the film resembles the natural photosynthetic light-harvesting complexes, albeit at much reduced efficacy. The decorated nanoparticles sensitize amorphous silicon photocells.     

Natural and artificial light-harvesting systems utilizing the functions of carotenoids

Carotenoids are essential pigments in natural photosynthesis. They absorb in the blue–green region of the solar spectrum and transfer the absorbed energy to (bacterio-)chlorophylls, and so expand the wavelength range of light that is able to drive photosynthesis. This process is an example of singlet–singlet energy transfer and so carotenoids serve to enhance the overall efficiency of photosynthetic light reactions. Carotenoids also act to protect photosynthetic organisms from the harmful effects of excess exposure to light. In this case, triplet–triplet energy transfer from (bacterio-)chlorophyll to carotenoid plays a key role in this photoprotective reaction. In the light-harvesting pigment–protein complexes from purple photosynthetic bacteria and chlorophytes, carotenoids have an additional role, namely the structural stabilization of those complexes. In this article we review what is currently known about how carotenoids discharge these functions. The molecular architecture of photosynthetic systems will be outlined to provide a basis from which to describe the photochemistry of carotenoids, which underlies most of their important functions in photosynthesis. Then, the possibility to utilize the functions of carotenoids in artificial photosynthetic light-harvesting systems will be discussed. Some examples of the model systems are introduced.     

Electron transfer rates and Franck–Condon factors: an application to the early electron transfer steps in photosynthetic reaction centers

Mechanistic aspects of some of the early electron transfer steps occurring in photosynthetic reaction centers are discussed. Starting from the normal modes of the redox cofactors involved in the electron transfer processes, we show how a series of quantities which regulate electron transfer rates, such as (i) the electron transfer active modes, (ii) the intramolecular reorganization energy, and (iii) the mutual couplings between the vibronic states of the donor and the acceptor, can be obtained and used to draw qualitative conclusions on ET rates.