Photosynthetic Light-harvesting Systems Research Articles

Effect of correlation of local fluctuations on exciton coherence

Recent experimental studies have shown both oscillations of exciton populations and long lasting coherence in multichromophoric systems such as photosynthetic light harvesting systems and conjugated polymers. It has been suggested that this quantum effect is due to correlations of the fluctuations of site energies among the closely packed chromophores in the protein environment. In addition to these, there is the strong possibility of correlations between site energies and transfer matrix elements. In order to understand the role of such correlations we generalize the Haken-Strobl-Reineker (HSR) model to include the energetic correlations and the site diagonal-off-diagonal correlations in a systematic way. The extended HSR model in the exciton basis is also constructed and allows us to study the dynamics of the exciton populations and coherences. With the extended model, we can provide insight into how these correlations affect the evolution of the populations and coherences of excitons by comparing to the original HSR model with uncorrelated fluctuating environments.

Efficient Light Harvesting by Photosystem II Requires an Optimized Protein Packing Density in Grana Thylakoids

A recently developed technique for dilution of the naturally high protein packing density in isolated grana membranes was applied to study the dependence of the light harvesting efficiency of photosystem (PS) II on macromolecular crowding. Slight dilution of the protein packing from 80% area fraction to the value found in intact grana thylakoids (70%) leads to an improved functionality of PSII (increased antenna size, enhanced connectivity between reaction centers). Further dilution induces a functional disconnection of light-harvesting complex (LHC) II from PSII. It is concluded that efficient light harvesting by PSII requires an optimal protein packing density in grana membranes that is close to 70%. We hypothesize that the decreased efficiency in overcrowded isolated grana thylakoids is caused by excited state quenching in LHCII, which has previously been correlated with neoxanthin distortion. Resonance Raman spectroscopy confirms this increase in neoxanthin distortion in overcrowded grana as compared with intact thylakoids. Furthermore, analysis of the changes in the antenna size in highly diluted membranes indicates a lipid-induced dissociation of up to two trimeric LHCII from PSII, leaving one trimer connected. This observation supports a hierarchy of LHCII-binding sites on PSII.

Identification of a single peridinin sensing Chl- a excitation in reconstituted PCP by crystallography and spectroscopy

The peridinin-chlorophyll a-protein (PCP) of dinoflagellates is unique among the large variety of natural photosynthetic light-harvesting systems. In contrast to other chlorophyll protein complexes, the soluble PCP is located in the thylakoid lumen, and the carotenoid pigments outnumber the chlorophylls. The structure of the PCP complex consists of two symmetric domains, each with a central chlorophyll a (Chl-a) surrounded by four peridinin molecules. The protein provides distinctive surroundings for the pigment molecules, and in PCP, the specific environment around each peridinin results in overlapping spectral line shapes, suggestive of different functions within the protein. One particular Per, Per-614, is hypothesized to show the strongest electronic interaction with the central Chl-a. We have performed an in vitro reconstitution of pigments into recombinant PCP apo-protein (RFPCP) and into a mutated protein with an altered environment near Per-614. Steady-state and transient optical spectroscopic experiments comparing the RFPCP complex with the reconstituted mutant protein identify specific amino acid-induced spectral shifts. The spectroscopic assignments are reinforced by a determination of the structures of both RFPCP and the mutant by x-ray crystallography to a resolution better than 1.5 A. RFPCP and mutated RFPCP are unique in representing crystal structures of in vitro reconstituted light-harvesting pigment-protein complexes.

Ultrafast exciton-exciton coherent transfer in molecular aggregates and its application to light-harvesting systems

Effects of the exciton-exciton coherence transfer (EECT) in strongly coupled molecular aggregates are investigated from the reduced time-evolution equation which we have developed to describe EECT. Starting with the nonlinear response function, we obtained explicit contributions from EECT to four-wave-mixing spectrum such as photon echo, taking into account double exciton states, static disorder, and heat-bath coupling represented by arbitrary spectral densities. By using the doorway-window picture and the projection operator technique, the transfer rates between two different electronic coherent states are obtained within a framework of cumulant expansion at high temperature. Applications of the present theory to strongly coupled B850 chlorophylls in the photosynthetic light harvesting system II (LH2) are discussed. It is shown that EECT is indispensable in properly describing ultrafast phenomena of strongly coupled molecular aggregates such as LH2 and that the EECT contribution to the two-dimensional optical spectroscopy is not negligible.

Coherence in the B800 Ring of Purple Bacteria LH2

We study the quantum coherence in the B800 ring and how it affects the dynamics of excitation energy transfer (EET) in photo-synthetic light-harvesting systems. From an analysis of the spectrum, we determine the disorder parameters for the B800 ring and show that the relatively weak electronic coupling between B800 pigments subtly changes the dynamics of EET and improves the uniformity and robustness of B800 --> B850 EET at room temperature, an example of how a multichromophoric assembly can exploit coherence to optimize the efficiency of photosynthesis. A molecular-level description for the dynamics of EET in the light-harvesting system may prove useful for understanding other nanoscale molecular assemblies and designing efficient nanoscale optical devices.

Self-aggregates of natural and modified chlorophylls as photosynthetic light-harvesting antenna systems: substituent effect on the B-ring

Extramembranous light-harvesting antennae called 'chlorosomes' are the main sunlight-absorbing and energy-migrating systems in photosynthetic green bacteria. In a chlorosome, specific chlorophyllous pigments self-aggregate in hydrophobic environments surrounded by a lipid monolayer to form large oligomers. The self-aggregates of chlorosomal chlorophylls possessing a chlorin pi-system absorb sunlight and can emit near-infrared light, which is transferred to a bacteriochlorin pigment situated in the chlorosomal surface membrane. In vivo and in vitro self-aggregates of natural chlorosomal chlorophylls and their models have been investigated by electronic absorption analysis. Here their self-aggregation is reviewed from the viewpoint of substituent effect on the pyrrolic B-ring. Substituents at the 7- and 8-positions did not disturb the formation of their self-aggregates but affected their absorption bands.

Photochromicity of Anabaena Sensory Rhodopsin, an Atypical Microbial Receptor with a cis-Retinal Light-adapted Form

We characterize changes in isomeric states of the retinylidene chromophore during light-dark adaptation and photochemical reactions of Anabaena (Nostoc) sp. PCC7120 sensory rhodopsin (ASR). The results show that ASR represents a new type of microbial rhodopsin with a number of unusual characteristics. The three most striking are: (i) a primarily all-trans configuration of retinal in the dark-adapted state and (ii) a primarily 13-cis light-adapted state with a blue-shifted and lower extinction absorption spectrum, opposite of the case of bacteriorhodopsin; and (iii) efficient reversible light-induced interconversion between the 13-cis and all-trans unphotolyzed states of the pigment. The relative amount of ASR with cis and trans chromophore forms depends on the wavelength of illumination, providing a mechanism for single-pigment color sensing analogous to that of phytochrome pigments. In addition ASR exhibits unusually slow formation of L-like and M-like intermediates, with a dominant accumulation of M during the photocycle. Co-expression of ASR with its putative cytoplasmic transducer protein shifts the absorption maximum and strongly decreases the rate of dark adaptation of ASR, confirming interaction between the two proteins. Thus ASR, the first non-haloarchaeal sensory rhodopsin characterized, demonstrates the diversity of photochemistry of microbial rhodopsins. Its photochromic properties and the position of its two ground state absorption maxima suggest it as a candidate for controlling differential photosynthetic light-harvesting pigment synthesis (chromatic adaptation) or other color-sensitive physiological responses in Anabaena cells.

Developing a Structure–Function Model for the Cryptophyte Phycoerythrin 545 Using Ultrahigh Resolution Crystallography and Ultrafast Laser Spectroscopy

Cryptophyte algae differ from cyanobacteria and red algae in the architecture of their photosynthetic light harvesting systems, even though all three are evolutionarily related. Central to cryptophyte light harvesting is the soluble antenna protein phycoerythrin 545 (PE545). The ultrahigh resolution crystal structure of PE545, isolated from a unicellular cryptophyte Rhodomonas CS24, is reported at both 1.1A and 0.97A resolution, revealing details of the conformation and environments of the chromophores. Absorption, emission and polarized steady state spectroscopy (298K, 77K), as well as ultrafast (20fs time resolution) measurements of population dynamics are reported. Coupled with complementary quantum chemical calculations of electronic transitions of the bilins, these enable assignment of spectral absorption characteristics to each chromophore in the structure. Spectral differences between the tetrapyrrole pigments due to chemical differences between bilins, as well as their binding and interaction with the local protein environment are described. Based on these assignments, and considering customized optical properties such as strong coupling, a model for light harvesting by PE545 is developed which explains the fast, directional harvesting of excitation energy. The excitation energy is funnelled from four peripheral pigments (beta158,beta82) into a central chromophore dimer (beta50/beta61) in approximately 1ps. Those chromophores, in turn, transfer the excitation energy to the red absorbing molecules located at the periphery of the complex in approximately 4ps. A final resonance energy transfer step sensitizes just one of the alpha19 bilins on a time scale of 22ps. Furthermore, it is concluded that binding of PE545 to the thylakoid membrane is not essential for efficient energy transfer to the integral membrane chlorophyll a-containing complexes associated with PS-II.

Photosynthetic antennae systems: energy transport and optical absorption

The energy transport and the optical line shape of molecular aggregates, modeling bacteria photosynthetic light-harvesting systems (chlorosomes in the case of Chlorobium tepidum or Chloroflexus aurantiacus and LH2 in the case of Rhodopseudomonas acidophila) is investigated theoretically. The molecular units are described by two-level systems with an average excitation energy ε and interacting with each other through nearest-neighbor interactions. For LH2 an elliptical deformation of the ring is also allowed. Furthermore, dynamic and in the case of LH2 also quasi-static fluctuations of the local excitation energies are taken into account, simulating fast molecular vibrations and slow motions of the protein backbone, respectively. The fluctuations are described by Gaussian Markov processes in the case of the chlorosomes and by colored dichotomic Markov processes, with exponentially decaying correlation functions, with small ( λ s) and large ( λ) decay constants, in the case of LH2.

Fluorescence spectroscopy of single photosynthetic light-harvesting supramolecular systems.

Recent spectroscopic studies of photosynthetic light-harvesting supramolecular complexes at the single supramolecule level are reviewed. This report describes the "single-molecule" investigation on light-harvesting complex 2 (LH2) of purple photosynthetic bacteria, phycobiliproteins of cyanobacteria and red algae, light-harvesting complex 2 (LHC2) of higher plants, and chlorosomes of green photosynthetic bacteria. Unique behaviors and spectral features of single light-harvesting apparatus have been unraveled that were hidden by the ensemble averaging of many of the complexes. The information obtained will be useful for understanding the electronic structures and energy-transfer mechanism of photosynthetic light-harvesting supramolecular systems.

Construction of kinetic domains in energy trapping processes and application to a photosynthetic light harvesting complex

We develop a formulation allowing construction of various kinetic domains from a master equation for population transfer dynamics and enabling calculation of the time scales of transition between such domains. In this way, a complicated network of energy transfer steps can be simplified to a series of sequential kinetic transitions over the kinetic domains. We illustrate the advantage of this formulation by applying it to energy trapping in a photosynthetic light harvesting system and as a result we obtain a clear picture of energy transfer dynamics and the various rate determining steps in Photosystem I.

Exciton dynamics in light harvesting systems

The optical line shape of molecular ring aggregates with 18 molecular units, modeling bacteria photo-synthetic light harvesting systems, is investigated theoretically. The molecular units are described by two-level systems with an average excitation energy ε and interacting with each other through nearest-neighbor interaction. Furthermore, quasi-static and dynamic fluctuations of the local excitation energies are taken into account simulating slow motions of the protein backbone and fast molecular vibrations, respectively. The fluctuations are described by colored dichotomic Markov processes with exponentially decaying correlation functions with small (λs) and large (λ) decay constants, respectively. The optical line shape is discussed in dependence of the model parameters including a possible elliptical deformation. Furthermore we investigate the coupled coherent and incoherent energy transport in chlorosomes.

Weakly coupled molecular photonic wires: synthesis and excited-state energy-transfer dynamics.

Molecular photonic wires, which absorb light and undergo excited-state energy transfer, are of interest as biomimetic models for photosynthetic light-harvesting systems and as molecular devices with potential applications in materials chemistry. We describe the stepwise synthesis of four molecular photonic wires. Each wire consists of an input unit, transmission element, and output unit. The input unit consists of a boron-dipyrrin dye or a perylene-monoimide dye (linked either at the N-imide or the C9 position); the transmission element consists of one or three zinc porphyrins affording short or long wires, respectively; and the output unit consists of a free base (Fb) porphyrin. The components in the arrays are joined in a linear architecture via diarylethyne linkers (an ethynylphenyl linker is attached to the C9-linked perylene). The wires have been examined by static absorption, static fluorescence, and time-resolved absorption spectroscopy. Each wire (with the exception of the C9-linked perylene wire) exhibits a visible absorption spectrum that is the sum of the spectra of the component parts, indicating the relatively weak electronic coupling between the components. Excitation of each wire at the wavelength where the input unit absorbs preferentially (typically 480-520 nm) results in emission almost exclusively from the Fb porphyrin. The static emission and time-resolved data indicate that the overall rate constants and quantum efficiencies for end-to-end (i.e., input to output) energy transfer are as follows: perylene-(N-imide)-linked short wire, (33 ps)(-1) and >99%; perylene-(C9)-linked short wire, (26 ps)(-1) and >99%; boron-dipyrrin-based long wire, (190 ps)(-1) and 81%; perylene-(N-imide)-linked long wire, (175 ps)(-1) and 86%. Collectively, the studies provide valuable insight into the singlet-singlet excited-state energy-transfer properties in weakly coupled molecular photonic wires.

Excitons in a photosynthetic light-harvesting system: a combined molecular dynamics, quantum chemistry, and polaron model study.

The dynamics of pigment-pigment and pigment-protein interactions in light-harvesting complexes is studied with an approach that combines molecular dynamics simulations with quantum chemistry calculations and a polaron model analysis. The molecular dynamics simulation of light-harvesting (LH) complexes was performed on an 87 055 atom system comprised of a LH-II complex of Rhodospirillum molischianum embedded in a lipid bilayer and surrounded with appropriate water layers. For each of the 16 B850 bacteriochlorophylls (BChls), we performed 400 ab initio quantum chemistry calculations on geometries that emerged from the molecular dynamical simulations, determining the fluctuations of pigment excitation energies as a function of time. From the results of these calculations we construct a time-dependent Hamiltonian of the B850 exciton system from which we determine within linear response theory the absorption spectrum. Finally, a polaron model is introduced to describe both the excitonic and coupled phonon degrees of freedom by quantum mechanics. The exciton-phonon coupling that enters into the polaron model, and the corresponding phonon spectral function, are derived from the molecular dynamics and quantum chemistry simulations. The model predicts that excitons in the B850 BChl ring are delocalized over five pigments at room temperature. Also, the polaron model permits the calculation of the absorption and circular dichroism spectra of the B850 excitons from the sole knowledge of the autocorrelation function of the excitation energies of individual BChls, which is readily available from the combined molecular dynamics and quantum chemistry simulations. The obtained results are found to be in good agreement with the experimentally measured absorption and circular dichroism spectra.

Exciton States and Relaxation in Molecular Aggregates: Numerical Study of Photosynthetic Light Harvesting

In this article we briefly review the molecular exciton theory and apply it to photosynthetic light harvesting systems. We derive expressions for exciton relaxation rates using perturbation theory in Hilbert space representation and show how the Forster equation can be obtained from a general relaxation rate expression in case of well localized excitons. A detailed analysis of the exciton level structure and wavefunctions of the ring structure is presented for diagonal and nondiagonal disorder. We conclude that the latter plays only a minor role in light-harvesting systems. We emphasize the relaxation rate dependency on square of the energy gap, which makes the high frequency modes particularly important for the exciton relaxation. We found a reasonably good agreement between the measured and calculated relaxation rates in photosynthetic purple bacteria.

Modeling excitonic line shapes of photosynthetic light harvesting systems: influence of quasi-static and dynamic disorder

The modeling of optical line shape of molecular ring aggregates with 9 and 18 molecular units of photosynthetic bacteria light-harvesting systems is investigated theoretically. The molecular units are described by two-level systems, with an average excitation energy ε, which interact with each other through nearest-neighbor interaction. A possible dimerization is taken into account by allowing for alternating strong ( J S) and weak ( J W) transfer integrals. Furthermore, quasi-static and dynamic fluctuations of the local excitation energies are taken into account simulating slow motions of the protein backbone and fast molecular vibrations, respectively. The fluctuations are described by colored dichotomic Markov processes with exponentially decaying correlation functions with small ( λ s) and large ( λ) decay constants, respectively. The optical line shape is discussed with respect to the model parameters.

Short-Range Coherence in the Energy Transfer of Photosynthetic Light-Harvesting Systems

We employ a simple model for the electronic excitations and the exciton-vibration coupling characterizing the B850 ring of the light-harvesting complex in photosynthetic bacteria to investigate the possibility of coherence in the energy transfer within the system. The structure of the equilibrium density matrix is studied using the path integral formulation of quantum statistical mechanics. The calculated mean coherence length is computed from the average root-mean-square deviation of closed imaginary time paths that are sampled via a Monte Carlo procedure. This procedure allows simultaneous examination of the effects of thermal averaging and dynamic and static disorder in a single calculation. The mean coherence length is found to be about two to three chlorophyll monomers at room temperature. The principal factor responsible for this localization is thermal averaging, although static and dynamic disorder further destabilize extended states. At low temperatures the circular arrangement of the pigments favors coherence with respect to the situation in a linear aggregate. Visual inspection of typical paths offers an intuitive picture of the extent of coherent energy delocalization in biological antenna systems.

Energy transfer between carotenoids and bacteriochlorophylls in light-harvesting complex II of purple bacteria

In photosynthetic light-harvesting systems carotenoids and chlorophylls jointly absorb light and transform its energy within about a picosecond into electronic singlet excitations of the chlorophylls only. This paper investigates this process for the light-harvesting complex II of the purple bacterium Rhodospirillum molischianum, for which a structure and, hence, the exact arrangement of the participating bacteriochlorophylls and carotenoids have recently become known. Based on this structure and on CI expansions of the electronic states of individual chromophores (bacteriochlorophylls and carotenoids) as well as on an exciton description of a circular aggregate of bacteriochlorophylls, the excitation transfer between carotenoids and bacteriochlorophylls is described by means of Fermi's golden rule. The electronic coupling between the various electronic excitations is determined for all orders of multipoles (Coulomb mechanism) and includes the electron exchange (Dexter mechanism) term. The rates and efficiencies for different pathways of excitation transfer, e.g., ${1}^{1}{B}_{u}^{+}(\mathrm{carotenoid})\ensuremath{\rightarrow}\mathrm{bacteriochlorophyll}$ aggregate and ${2}^{1}{A}_{g}^{\ensuremath{-}}(\mathrm{carotenoid})\ensuremath{\rightarrow}\mathrm{}\mathrm{bacteriochlorophyll}$ aggregate, are compared. The results show that in LH-II the Coulomb mechanism is dominant for the transfer of singlet excitations. The ${1}^{1}{B}_{u}^{+}\ensuremath{\rightarrow}{Q}_{x}$ pathway appears to be partially efficient, while the ${2}^{1}{A}_{g}^{\ensuremath{-}}\ensuremath{\rightarrow}{Q}_{y}$ pathway, in our description, which does not include vibrational levels, is inefficient. An improved treatment of the excitation transfer from the ${2}^{1}{A}_{g}^{\ensuremath{-}}$ state is required to account for observed transfer rates. Exciton splitting of bacteriochlorophyll ${Q}_{y}$ excitations slightly accelerates the excitation transfer from the ${2}^{1}{A}_{g}^{\ensuremath{-}}$ state, while it plays a crucial role in accelerating the transfer from the $B800\mathrm{BChl}{Q}_{y}$ state. Photoprotection of bacteriochlorophylls through triplet quenching is investigated, too. The results suggest that eight of the $16B850$ bacteriochlorophylls in LH-II of Rhodospirillum molischianum are protected well by eight carotenoids observed in the x-ray structure of the protein. The remaining eight $B850$ bacteriochlorophylls can transfer their triplet excitation energy efficiently to their neighboring protected bacteriochlorophylls. Eight $B800$ bacteriochlorophylls appear not to be protected well by the observed carotenoids.

Femtosecond spectroscopy of photosynthetic light-harvesting systems

Observing the elementary steps of light-harvesting in real time is now possible using femtosecond spectroscopy. This, combined with new structural data, has allowed a fairly complete description of light-harvesting in purple bacteria and substantial insights into higher plant antenna systems.

Superradiance and Exciton Delocalization in Bacterial Photosynthetic Light-Harvesting Systems

We present temperature-dependent fluorescence quantum yield and lifetime measurements on the LH-1 and LH-2 complexes of Rhodobacter sphaeroides and on the isolated B820 subunit of Rhodospirillum rubrum. From these measurements the superradiance is calculated, which is related to the delocalization of excitations in these complexes. In the B820 preparation we find a radiative rate that is 30% higher than that of monomeric bacteriochlorophyll, in agreement with a dimer model of this subunit. At room temperature both LH-1 and LH-2 are superradiant relative to monomeric Bchl-a with enhancement factors of 3.8 and 2.8, respectively. In LH-2 the radiative rate does not change significantly upon lowering the temperature to 4 K. LH-1 however exhibits a strong temperature dependence, giving rise to a 2.4 times higher radiative rate at 4 K relative to room temperature. From modeling of the superradiance using a Hamiltonian based on the LH-2 structure and including site inhomogeneity, we conclude that the ratio of in...