Chlorophyll Dimer Research Articles

Novel Conjugates of Galactose with Dimeric Chlorophyll a Derivatives

Novel Conjugates of Galactose with Dimeric Chlorophyll a Derivatives

Photochemical reactions of chlorophyll tetramer in water-soluble chlorophyll-binding protein BoWSCP

The absorption dynamics of chlorophyll a in a symmetric tetrameric complex of the water-soluble chlorophyll-binding protein BoWSCP was measured by the broadband femtosecond laser pump-probe spectroscopy within the range from 400 to 780 nm with a time resolution of 20 f-200 ps. When BoWSCP was excited in the region of the Soret band at a wavelength of 430 nm, a nonradiative intramolecular conversion S3 → S1 was observed with a characteristic time of 83 ± 9 fs. When the complex was excited in the region of the Qy band at a wavelength of 670 nm, a relaxation transition between two excitonic states of the chlorophyll dimer was observed with a time of 105 ± 10 fs. Absorption spectra of excited singlet states S1 and S3 of chlorophyll a were obtained. It has been demonstrated that the delocalization of the excited state between exciton-coupled Chl molecules in the BoWSCP tetramer changes in time and depends on the excitation energy. Upon excitation of BoWSCP, an ultrafast photochemical reaction is observed in the Soret region, apparently due to the reduction of tryptophan in the vicinity of chlorophyll.

Femtosecond Dynamics of Excited States of Chlorophyll Tetramer in Water-Soluble Chlorophyll-Binding Protein BoWSCP.

The paper reports on the absorption dynamics of chlorophyll a in a symmetric tetrameric complex of the water-soluble chlorophyll-binding protein BoWSCP. It was measured by a broadband femtosecond laser pump-probe spectroscopy within the range from 400 to 750 nm and with a time resolution of 20 fs-200 ps. When BoWSCP was excited in the region of the Soret band at a wavelength of 430 nm, nonradiative intramolecular conversion S3→S1 was observed with a characteristic time of 83 ± 9 fs. When the complex was excited in the region of the Qy band at 670 nm, relaxation transition between two excitonic states of the chlorophyll dimer was observed in the range of 105 ± 10 fs. Absorption spectra of the excited singlet states S1 and S3 of chlorophyll a were obtained. The delocalization of the excited state between exciton-coupled Chl molecules in BoWSCP tetramer changed in time and depended on the excitation energy. When BoWSCP is excited in the Soret band region, an ultrafast photochemical reaction is observed. This could result from the reduction of tryptophan in the vicinity of chlorophyll.

Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I.

The antenna complexes of Photosystem I present low-lying states visible as red-shifted and broadened absorption and fluorescence bands. Among these, Lhca4 has the most evident features of these "red" states, with a fluorescence band shifted by more than 25 nm from typical LHC emission. This signal arises from a mixing of exciton and charge-transfer (CT) states within the excitonically coupled a603-a609 chlorophyll (Chl) dimer. Here we combine molecular dynamics, multiscale quantum chemical calculations, and spectral simulations to uncover the molecular mechanism for the formation and tuning of exciton-CT interactions in Lhca4. We show that the coupling between exciton and CT states is extremely sensitive to tiny variations in the Chl dimer arrangement, explaining both the red-shifted bands and the switch between conformations with blue and red emission observed in single-molecule spectroscopy. Finally, we show that mutating the axial ligand of a603 diminishes the exciton-CT coupling, removing any red-state fingerprint.

Extracting the excitonic Hamiltonian of a chlorophyll dimer from broadband two-dimensional electronic spectroscopy.

We apply Frenkel exciton theory to model the entire Q-band of a tightly bound chlorophyll dimer inspired by the photosynthetic reaction center of photosystem II. The potential of broadband two-dimensional electronic spectroscopy experiment spanning the Qx and Qy regions to extract the parameters of the model dimer Hamiltonian is examined through theoretical simulations of the experiment. We find that the local nature of Qx excitation enables identification of molecular properties of the delocalized Qy excitons. Specifically, we demonstrate that the cross-peak region, where excitation energy is resonant with Qy while detection is at Qx, contains specific spectral signatures that can reveal the full real-space molecular Hamiltonian, a task that is impossible by considering the Qy transitions alone. System-bath coupling and site energy disorder in realistic systems may limit the resolution of these spectral signatures due to spectral congestion.

Ring-shaped self-assembly of a naphthalene-linked chlorophyll dimer.

Light-harvesting antennas, for example the LH2 complex in purple bacteria, sophisticatedly align chlorophyll molecules in a cyclic fashion by using protein scaffolds. However, artificial preparation of the circular LH antenna model without any templates has not been reported. We demonstrated the construction of ring-shaped supramolecules by self-assembly of a semisynthetic chlorophyll dimer through a transformation from wavy fiber-like aggregates.

Quasiparticle Self-Consistent GW-Bethe-Salpeter Equation Calculations for Large Chromophoric Systems.

The GW-Bethe-Salpeter equation (BSE) method is promising for calculating the low-lying excitonic states of molecular systems. However, so far it has only been applied to rather small molecules and in the commonly implemented diagonal approximations to the electronic self-energy, it depends on a mean-field starting point. We describe here an implementation of the self-consistent and starting-point-independent quasiparticle self-consistent (qsGW)-BSE approach, which is suitable for calculations on large molecules. We herein show that eigenvalue-only self-consistency can lead to an unfaithful description of some excitonic states for chlorophyll dimers while the qsGW-BSE vertical excitation energies (VEEs) are in excellent agreement with spectroscopic experiments for chlorophyll monomers and dimers measured in the gas phase. Furthermore, VEEs from time-dependent density functional theory calculations tend to disagree with experimental values and using different range-separated hybrid (RSH) kernels does change the VEEs by up to 0.5 eV. We use the new qsGW-BSE implementation to calculate the lowest excitation energies of the six chromophores of the photosystem II (PSII) reaction center (RC) with nearly 2000 correlated electrons. Using more than 11,000 (6000) basis functions, the calculation could be completed in less than 5 (2) days on a single modern compute node. In agreement with previous TD-DFT calculations using RSH kernels on models that also do not include environmental effects, our qsGW-BSE calculations only yield states with local characters in the low-energy spectrum of the hexameric complex. Earlier works with RSH kernels have demonstrated that the protein environment facilitates the experimentally observed interchromophoric charge transfer. Therefore, future research will need to combine correlation effects beyond TD-DFT with an explicit treatment of environmental electrostatics.

Signatures of intramolecular vibrational and vibronic Q_{mathrm{x}}–Q_{mathrm{y}} coupling effects in absorption and CD spectra of chlorophyll dimers

An electron-vibrational coupling model that includes the vibronic (non-adiabatic) coupling between the Q_{mathrm{y}} and Q_{mathrm{x}} transitions of chlorophyll (Chl), created by Reimers and coworkers (Scientific Rep. 3, 2761, 2013) is extended here to chlorophyll dimers with interchlorophyll excitonic coupling. The model is applied to a Chl a dimer of the water-soluble chlorophyll binding protein (WSCP). As for isolated chlorophyll, the vibronic coupling is found to have a strong influence on the high-frequency vibrational sideband in the absorption spectrum, giving rise to a band splitting. In contrast, in the CD spectrum the interplay of vibronic coupling and static disorder leads to a strong suppression of the vibrational sideband in excellent agreement with the experimental data. The conservative nature of the CD spectrum in the low-energy region is found to be caused by a delicate balance of the intermonomer excitonic coupling between the purely electronic Q_{mathrm{y}} transition and the Q_{mathrm{y}} transition involving intramolecular vibrational excitations on one hand and the coupling to higher-energy electronic transitions on the other hand.

Towards the description of charge transfer states in solubilised LHCII using subsystem DFT

Light harvesting complex II (LHCII) in plants and green algae have been shown to adapt their absorption properties, depending on the concentration of sunlight, switching between a light harvesting and a non-harvesting or quenched state. In a recent work, combining classical molecular dynamics (MD) simulations with quantum chemical calculations (Liguori et al. in Sci Rep 5:15661, 2015) on LHCII, it was shown that the Chl611–Chl612 cluster of the terminal emitter domain can play an important role in modifying the spectral properties of the complex. In that work the importance of charge transfer (CT) effects was highlighted, in re-shaping the absorption intensity of the chlorophyll dimer. Here in this work, we investigate the combined effect of the local excited (LE) and CT states in shaping the energy landscape of the chlorophyll dimer. Using subsystem Density Functional Theory over the classical mus MD trajectory we look explicitly into the excitation energies of the LE and the CT states of the dimer and their corresponding couplings. Upon doing so, we observe a drop in the excitation energies of the CT states, accompanied by an increase in the couplings between the LE/LE and the LE/CT states facilitated by a shorter interchromophoric distance upon equilibration. Both these changes in conjunction, effectively produces a red-shift of the low-lying mixed exciton/CT states of the supramolecular chromophore pair.

Shedding light on primary donors in photosynthetic reaction centers

The light-induced transition from one or more neutral molecules into a tandem of charged species undergirds the photosynthetic process and thus the entirety of life as we know it. The charge separation reaction and subsequent transfer of electrons generates a series of transient charged species in the core of the photosynthetic reaction centers (RCs). While the mechanism of charge separation remains under investigation, it is known that the primary donor is key to the process. The primary donor is an excitonically coupled dimer of (bacterio)chlorophyll ((B)Chl) molecules located on the luminal side of RCs.

A dimeric chlorophyll electron acceptor differentiates type I from type II photosynthetic reaction centers

SummaryThis research addresses one of the most compelling issues in the field of photosynthesis, namely, the role of the accessory chlorophyll molecules in primary charge separation. Using a combination of empirical and computational methods, we demonstrate that the primary acceptor of photosystem (PS) I is a dimer of accessory and secondary chlorophyll molecules, Chl2A and Chl3A, with an asymmetric electron charge density distribution. The incorporation of highly coupled donors and acceptors in PS I allows for extensive delocalization that prolongs the lifetime of the charge-separated state, providing for high quantum efficiency. The discovery of this motif has widespread implications ranging from the evolution of naturally occurring reaction centers to the development of a new generation of highly efficient artificial photosynthetic systems.Video abstract

Understanding the Relation between Structural and Spectral Properties of Light-Harvesting Complex II.

Light-harvesting complex II (LHCII) is a pigment–protein complex present in higher plants and green algae. LHCII represents the main site of light absorption, and its role is to transfer the excitation energy toward the photosynthetic reaction centers, where primary energy conversion reactions take place. The optical properties of LHCII are known to depend on protein conformation. However, the relation between the structural and spectroscopic properties of the pigments is not fully understood yet. In this respect, previous classical molecular dynamics simulations of LHCII in a model membrane [Sci. Rep.2015, 5, 1–10] have shown that the configuration and excitonic coupling of a chlorophyll (Chl) dimer functioning as the main terminal emitter of the complex are particularly sensitive to conformational changes. Here, we use quantum chemistry calculations to investigate in greater detail the effect of pigment–pigment interactions on the excited-state landscape. While most previous studies have used a local picture in which electrons are localized on single pigments, here we achieve a more accurate description of the Chl dimer by adopting a supramolecular picture where time-dependent density functional theory is applied to the whole system at once. Our results show that specific dimer configurations characterized by shorter inter-pigment distances can result in a sizable intensity decrease (up to 36%) of the Chl absorption bands in the visible spectral region. Such a decrease can be predicted only when accounting for Chl–Chl charge-transfer excitations, which is possible using the above-mentioned supramolecular approach. The charge-transfer character of the excitations is quantified by two types of analyses: one focusing on the composition of the excitations and the other directly on the observable total absorption intensities.

Structure of the far-red light utilizing photosystem I of Acaryochloris marina

Acaryochloris marina is one of the cyanobacterial species that can use far-red light to drive photochemical reactions for oxygenic photosynthesis. Here, we report the structure of A. marina photosystem I (PSI) reaction center, determined by cryo-electron microscopy at 2.58 Å resolution. The structure reveals an arrangement of electron carriers and light-harvesting pigments distinct from other type I reaction centers. The paired chlorophyll, or special pair (also referred to as P740 in this case), is a dimer of chlorophyll d and its epimer chlorophyll d′. The primary electron acceptor is pheophytin a, a metal-less chlorin. We show the architecture of this PSI reaction center is composed of 11 subunits and we identify key components that help explain how the low energy yield from far-red light is efficiently utilized for driving oxygenic photosynthesis.

Supramolecular Nanofibers Constructed by Hydrogen Bonding of Chlorophyll Dimer

Chlorophyll pigments often assemble in a poor solvent to form less-ordered amorphous aggregates, despite the in vitro self-aggregation observed with chemically modified chlorophyll derivatives biomimicking a chlorosome. Chlorophyll dimer linked with a terephthalamide formed well-defined fiber shaped aggregates in hexane. The nanofiber was constructed by columnar self-aggregation via hydrogen bonding between terephthalamide moieties, which is different from chlorosomal aggregates that typically are formed by a coordination as well as hydrogen bonding.

Analysis of the electronic structure of the primary electron donor of photosystem I of <i>Spirodela</i> <i>oligorrhiza</i> by photochemically induced dynamic nuclear polarization (photo-CIDNP) solid-state nuclear magnetic resonance (NMR)

Abstract. The electron donor in photosystem I (PSI), the chlorophyll dimer P700, is studied by photochemically induced dynamic nuclear polarization (photo-CIDNP) magic angle spinning (MAS) nuclear magnetic resonance (NMR) on selectively 13C and uniformly 15N labeled PSI core preparations (PSI-100) obtained from the aquatic plant duckweed (Spirodela oligorrhiza). Light-induced signals originate from the isotope-labeled nuclei of the cofactors involved in the spin-correlated radical pair forming upon light excitation. Signals are assigned to the two donor cofactors (Chl a and Chl a') and the two acceptor cofactors (both Chl a). Light-induced signals originating from both donor and acceptor cofactors demonstrate that electron transfer occurs through both branches of cofactors in the pseudo-C2 symmetric reaction center (RC). The experimental results supported by quantum chemical calculations indicate that this functional symmetry occurs in PSI despite similarly sized chemical shift differences between the cofactors of PSI and the functionally asymmetric special pair donor of the bacterial RC of Rhodobacter sphaeroides. This contributes to converging evidence that local differences in time-averaged electronic ground-state properties, over the donor are of little importance for the functional symmetry breaking across photosynthetic RC species.

Absorption shifts of diastereotopically ligated chlorophyll dimers of photosystem I

The light-harvesting chlorophyll (Chl) molecules of photosynthetic systems form the basis for light-driven energy conversion. In biological environments, the Chl chromophores occur in two distinct diastereotopic configurations, where the α and β configurations have a magnesium-ligating histidine residue and a 17-propionic acid moiety on the opposite side or on the same side of the Chl ring, respectively. Although β-ligated Chl dimers occupy conserved positions around the reaction center of photosystem I (PSI), the functional relevance of the α/β configuration of the ligation is poorly understood. We employ here correlated ab initio calculations using the algebraic-diagrammatic construction through second order (ADC(2)) and the approximate second-order coupled cluster (CC2) methods in combination with the reduced virtual space (RVS) approach in studies of the intrinsic excited-state properties of α-ligated and β-ligated Chl dimers of PSI. Our ab initio calculations suggest that the absorption of the α-ligated reaction-center Chl dimer of PSI is redshifted by 0.13-0.14 eV in comparison to the β-ligated dimers due to combined excitonic coupling and strain effects. We also show that time-dependent density functional theory (TDDFT) calculations using range-separated density functionals underestimate the absorption shift between the α- and β-ligated dimers. Our findings may provide a molecular starting point for understanding the energy flow in natural photosynthetic systems, as well as a blueprint for developing new molecules that convert sunlight into other forms of energy.

Identification of Short- and Long-Wavelength Emitting Chlorophylls in Cyanobacterial Photosystem I by Plasmon-Enhanced Single-Particle Spectroscopy at Room Temperature.

A peculiarity of cyanobacterial Photosystem I (PSI) is the presence of so-called red chlorophylls absorbing at wavelengths longer than the reaction center P700. The origin and function of these chlorophylls have been debated in literature, but so far no consensus has been reached on either question. Here, we use plasmon-enhanced single-particle fluorescence spectroscopy to elucidate the origin of both short- and long-wavelength emitting species in monomeric PSI from Thermosynechococcus elongatus at room temperature. Polarized fluorescence spectra of single PSI complexes reveal a phase shift in the modulation of the short-wavelength (687 nm) and long-wavelength (717 nm) peaks. Numerical simulations show that this phase shift reflects a spatial angle of 15° between the transition dipole moments of the two forms. Quantum chemical calculations, together with reported X-ray structural and spectroscopic data, were used to assign the chlorophyll a monomer A3 as a candidate for the short-wavelength emitter and the B31-B32 chlorophyll dimer as a candidate for the long-wavelength emitter.

Triplet-Triplet Coupling in Chromophore Dimers: Theory and Experiment.

Knowledge of triplet state energies and triplet-triplet (T-T) interactions in aggregated organic molecules is essential for understanding photochemistry and dynamics of many natural and artificial systems. In this work, we combine direct phosphorescence measurements of triplet state energies, which are challenging due to the spin-forbidden nature of respective transitions and applicable to only a limited number of systems, with quantum chemical computational tools that can provide valuable qualitative and quantitative information about triplet states of interacting molecules. Using hexatriene, protoporphyrin, pheophorbide, and chlorophyll dimers as model systems, we demonstrate a complicated dependence of T-T coupling on a relative orientation of chromophores, governed by a nodal structure of overlapping electronic wave functions, that modulates interpigment interactions by orders of magnitude. It is also shown that geometrical relaxation of the triplet state is one of the critical factors for predictive modeling of T-T interactions in molecular aggregates.

Mechanism of adiabatic primary electron transfer in photosystem I: Femtosecond spectroscopy upon excitation of reaction center in the far-red edge of the QY band

The ultrafast primary charge separation in Photosystem I (PS I) excited by femtosecond pulses centered at 720 and 760nm was studied by pump-to-probe laser spectroscopy. The absorbance in the red edge of PS I absorption spectrum has an unusual exponential dependence on wavelength. The cutoff of short wavelength components of 760nm pulse allows direct excitation of reaction center chlorophyll molecules without involvement of light-harvesting antenna. The transient spectrum manifests the features of the primary ion-radical pair P700+A0− at time delay <180fs, followed by formation of the secondary pair P700+A1− with a characteristic time of 26ps. The obtained data are rationalized in the framework of adiabatic three-state model that includes the chlorophyll dimer P700 and two symmetrically arranged nearest chlorophyll molecules of A0. The arrangement of chlorophylls results in strong electronic coupling between P700 and A0. Excitation in the maximum of P700 absorption generates electronic states with the highest contribution from P700*, whereas excitation in the far-red edge predominantly generates charge transfer state P700+A0− in both branches of redox-cofactors. The three-level model accounts for a flat-bottomed potential surface of the excited state and adiabatic character of electron transfer between P700 and A0, providing a microscopic explanation of the ultrafast formation of P700+A0− and exponential decline of PS I absorption.

Coordination-Driven Dimerization of Zinc Chlorophyll Derivatives Possessing a Dialkylamino Group.

Zinc chlorophyll derivatives Zn-1-3 possessing a tertiary amino group at the C31 position have been synthesized through reductive amination of methyl pyropheophorbide-d obtained from naturally occurring chlorophyll-a. In a dilute CH2 Cl2 solution as well as in a dilute 10 %(v/v) CH2 Cl2 /hexane solution, Zn-1 possessing a dimethylamino group at the C31 position showed red-shifted UV/Vis absorption and intensified exciton-coupling circular dichroism (CD) spectra at room temperature owing to its dimer formation via coordination to the central zinc by the 31 -N atom of the dimethylamino group. However, Zn-2/3 bearing 31 -ethylmethylamino/diethylamino groups did not. The difference was dependent on the steric factor of the substituents in the tertiary amino group, where an increase of the carbon numbers on the N atom reduced the intermolecular N⋅⋅⋅Zn coordination. UV/Vis, CD, and 1 H NMR spectroscopic analyses including DOSY measurements revealed that Zn-1 formed closed-type dimers via an opened dimer by single-to-double axial coordination with an increase in concentration and a temperature decrease in CH2 Cl2 , while Zn-2/3 gave open and flexible dimers in a concentrated CH2 Cl2 solution at low temperature. The supramolecular closed dimer structures of Zn-1 were estimated by molecular modelling calculations, which showed these structures were promising models for the chlorophyll dimer in a photosynthetic reaction center.