Artificial Light-harvesting Complexes Research Articles

Experimental and computational characterisation of an artificial light harvesting complex.

Photosynthesis has been shown to be a highly efficient process for energy transfer in plants and bacteria. Like natural photosynthetic systems, the artificial light harvesting complex (LHC) BODIPY pillar[5]arene exhibits Förster resonance energy transfer (FRET). However, extensive characterisation of the BODIPY pillar[5]arene LHC to determine its suitability as an artificial LHC has yet to occur. In this paper we experimentally and computationally investigate the photophysical properties of the LHC by comparing the light absorption of the BODIPY LHC to individual BODIPY chromophores. Our results show evidence for quantum coherence, with oscillation frequencies of 100 cm-1 and 600 cm-1, which are attributable to vibronic, or exciton-phonon type coupling. Computational analysis suggests strong couplings of the molecular orbitals of the LHC resulting from the stacking of neighbouring BODIPY chromophore units. Interestingly, we find a 40% reduction in the absorbance of light for the BODIPY LHC compared to the individual chromophores which we attribute to electronic interactions between the conjugated π-systems of the BODIPY chromophores and the pillar[5]arene backbone.

Supramolecular assembly of pyrene-DNA conjugates: influence of pyrene substitution pattern and implications for artificial LHCs.

The supramolecular self-assembly of pyrene-DNA conjugates into nanostructures is presented. DNA functionalized with different types of pyrene isomers at the 3'-end self-assemble into nano-objects. The shape of the nanostructures is influenced by the type of pyrene isomer appended to the DNA. Multilamellar vesicles are observed with the 1,6- and 1,8-isomers, whereas conjugates of the 2,7-isomer exclusively assemble into spherical nanoparticles. Self-assembled nano-spheres obtained with the 2,7-dialkynyl pyrene isomer were used for the construction of an artificial light-harvesting complex (LHC) in combination with Cy3 as the energy acceptor.

Cryogenic TEM imaging of artificial light harvesting complexes outside equilibrium

The energy transport in natural light-harvesting complexes can be explored in laboratory conditions via self-assembled supramolecular structures. One such structure arises from the amphiphilic dye C8S3 molecules, which self-assemble in an aqueous medium to a double-wall cylindrical nanotube reminiscent of natural light-harvesting complexes found in green sulphur bacteria. In this paper, we report a way to investigate the structure of inner nanotubes (NTs) alone by dissolving the outer NTs in a microfluidic setting. The resulting thermodynamically unstable system was rapidly frozen, preventing the reassembly of the outer NT from the dissolved molecules, and imaged using cryogenic transmission electron microscopy (cryo-TEM). The experimental cryo-TEM images and the molecular structure were compared by simulating high-resolution TEM images, which were based on the molecular modelling of C8S3 NTs. We found that the inner NT with outer walls removed during the flash-dilution process had a similar size to the parent double-walled NTs. Moreover, no structural inhomogeneity was observed in the inner NT after flash-dilution. This opens up exciting possibilities for functionalisation of inner NTs before the reassembly of the outer NT occurs, which can be broadly extended to modify the intra-architecture of other self-assembled nanostructures.

Delocalized Two-Exciton States in DNA Scaffolded Cyanine Dimers.

The engineering and manipulation of delocalized molecular exciton states is a key component for artificial biomimetic light harvesting complexes as well as alternative circuitry platforms based on exciton propagation. Here we examine the consequences of strong electronic coupling in cyanine homodimers on DNA duplex scaffolds. The most closely spaced dyes, attached to positions directly across the double-helix from one another, exhibit pronounced Davydov splitting due to strong electronic coupling. We demonstrate that the DNA scaffold is sufficiently robust to support observation of the transition from the lowest energy (J-like) one-exciton state to the nonlocal two-exciton state, where each cyanine dye is in the excited state. This transition proceeds via sequential photon absorption and persists for the lifetime of the exciton, establishing this as a controlled method for creating two-exciton states. Our observations suggest that DNA-organized dye networks have potential as platforms for molecular logic gates and entangled photon emission based on delocalized two-exciton states.

Interplay between structural hierarchy and exciton diffusion in artificial light harvesting

Unraveling the nature of energy transport in multi-chromophoric photosynthetic complexes is essential to extract valuable design blueprints for light-harvesting applications. Long-range exciton transport in such systems is facilitated by a combination of delocalized excitation wavefunctions (excitons) and exciton diffusion. The unambiguous identification of the exciton transport is intrinsically challenging due to the system’s sheer complexity. Here we address this challenge by employing a spectroscopic lab-on-a-chip approach: ultrafast coherent two-dimensional spectroscopy and microfluidics working in tandem with theoretical modeling. We show that at low excitation fluences, the outer layer acts as an exciton antenna supplying excitons to the inner tube, while under high excitation fluences the former converts its functionality into an exciton annihilator which depletes the exciton population prior to any exciton transfer. Our findings shed light on the excitonic trajectories across different sub-units of a multi-layered artificial light-harvesting complex and underpin their great potential for directional excitation energy transport.

Triplet state quenching of bacteriochlorophyll c aggregates in a protein-free environment of a chlorosome interior

Efficient quenching of (bacterio)chlorophyll triplet states by carotenoids prevents formation of reactive singlet oxygen in photosynthetic light-harvesting complexes. This protective process requires a close interaction between both types of pigments, which is usually ensured by a protein scaffold. Here we have studied quenching of bacteriochlorophyll c triplets in chlorosomes from the green photosynthetic bacterium Chloroflexus aurantiacus by nanosecond spectroscopy. Bacteriochlorophyll c forms aggregates in the chlorosome interior without involvement of a protein. We have observed that the triplet transfer from bacteriochlorophyll aggregates to carotenoids occurs with a transfer time of approximately 4 ns, being more than ten times slower that the estimates for the fastest triplet quenching in pigment-protein light-harvesting complexes. Nevertheless, together with aggregation-mediated shortening of excited state lifetimes, carotenoids provide efficient protection against formation of singlet oxygen in chlorosomes. Efficient triplet quenching was also observed in self-assembling, artificial light-harvesting complexes containing bacteriochlorophyll c aggregates and β-carotene. This is important for their future applications in solar energy conversion. Finally, we have studied the temperature dependence of triplet quenching in chlorosomes and determined the activation energy of the energy transfer to be about 0.08 eV. This value lies within the range estimated for pigment-protein light-harvesting complexes.

Excimer Formation in Carboxylic Acid-Functionalized Perylene Diimides Attached to Silicon Dioxide Nanoparticles.

The creation of artificial light-harvesting complexes involves the ordered arrangement of chromophores in space. To guarantee efficient energy-transfer processes, organic dyes must be brought into close proximity, often leading to aggregation and the formation of excimer states. In recent years, the attachment of ligand-based chromophores to nanoparticles has also generated interest in relation to improved solar harvesting and spin-dependent electronic interactions such as singlet fission and upconversion. We explore the covalent attachment of two novel perylene-diimide (PDI) carboxylic acid ligands to silicon dioxide nanoparticles. This allows us to study electronic interactions between the ligands when attached to nanoparticles because these cannot couple to the wide band gap silicon dioxide. One of the synthesized PDI ligands has sterically hindering phenols in the bay position and undergoes minimal optical changes upon attachment, but the other forms an excimer state with a red-shifted and long-lived florescence. As such, molecular structure changes offer a method to tune weak and strong interactions between ligand layers on nanocrystal surfaces.

Porphyrin Boxes.

In order to fabricate efficient molecular photonic devices, it has been a long-held aspiration for chemists to understand and mimic natural light-harvesting complexes where a rapid and efficient transfer of excitation energy between chlorophyll pigments is observed. Synthetic porphyrins are attractive building blocks in this regard because of their rigid and planar geometry, high thermal and electronic stability, high molar extinction, small and tunable band gap, and tweakable optical as well as redox behavior. Owing to these fascinating properties, various types of porphyrin-based architectures have been reported utilizing both covalent and noncovalent approaches. However, it still remains a challenge to construct chemically robust, well-defined three-dimensional porphyrin cages which can be easily synthesized and yet suitable for useful applications both in solution as well as in solid state. Working on this idea, we recently synthesized box-shaped organic cages, which we called porphyrin boxes, by making use of dynamic covalent chemistry of imine condensation reaction between 4-connecting, square-shaped, tetraformylporphyrin and 3-connecting, triangular-shaped, triamine molecules. Various presynthetic, as well as postsynthetic modifications, can be carried out on porphyrin boxes including a variation of the alkyl chain length in their 3-connecting subunit, chemical functionalization, and metalation of the porphyrin core. This can remarkably tune their inherent properties, e.g., solubility, window size, volume, and polarity of the internal void. The porphyrin boxes can therefore be considered as a significant addition to the family of multiporphyrin-based architectures, and because of their chemical stability and shape persistency, the applications of porphyrin boxes expand beyond the photophysical properties of an artificial light-harvesting complex. Consequently, they have been exploited as porous organic cages, where their gas adsorption properties have been investigated. By incorporating them in a lipid bilayer membrane, an iodide selective synthetic ion channel has also been demonstrated. Further, we have explored electrocatalytic reduction of carbon dioxide using Fe(III) metalated porphyrin boxes. Additionally, the precise size and ease of metalation of porphyrin boxes allowed us to utilize them as premade building blocks for creating coordination-based hierarchical superstructures. Considering these developments, it may be worth combining the photophysical properties of porphyrin with the shape-persistent porous nature of porphyrin boxes to explore other novel applications. This Account summarizes our recent work on porphyrin boxes, starting with their design, structural features, and applications in different fields. We also try to provide scientific insight into the future opportunities that these amazing boxes have in store for exploring the still uncharted challenging domains in the field of supramolecular chemistry in a confined space.

FRET efficiency and antenna effect in multi-color DNA origami-based light harvesting systems

Artificial light harvesting complexes find applications in photosynthesis, photovoltaics and chemical sensors. Here, we present the characterization and optimization of a multi-color artificial light harvesting system on DNA origami structures.

Surface-Cross-Linked Micelles as Multifunctionalized Organic Nanoparticles for Controlled Release, Light Harvesting, and Catalysis.

Surfactant micelles are dynamic entities with a rapid exchange of monomers. By “clicking” tripropargylammonium-containing surfactants with diazide cross-linkers, we obtained surface-cross-linked micelles (SCMs) that could be multifunctionalized for different applications. They triggered membrane fusion through tunable electrostatic interactions with lipid bilayers. Antenna chromophores could be installed on them to create artificial light-harvesting complexes with efficient energy migration among tens to hundreds of chromophores. When cleavable cross-linkers were used, the SCMs could break apart in response to redox or pH signals, ejecting entrapped contents quickly as a result of built-in electrostatic stress. They served as caged surfactants whose surface activity was turned on by environmental stimuli. They crossed cell membranes readily. Encapsulated fluorophores showed enhanced photophysical properties including improved quantum yields and greatly expanded Stokes shifts. Catalytic groups could be installed on the surface or in the interior, covalently attached or physically entrapped. As enzyme mimics, the SCMs enabled rational engineering of the microenvironment around the catalysts to afford activity and selectivity not possible with conventional catalysts.

Possible role of interference, protein noise, and sink effects in nonphotochemical quenching in photosynthetic complexes.

We analyze theoretically a simple and consistent quantum mechanical model that reveals the possible role of quantum interference, protein noise, and sink effects in the nonphotochemical quenching (NPQ) in light-harvesting complexes (LHCs). The model consists of a network of five interconnected sites (excitonic states of light-sensitive molecules) responsible for the NPQ mechanism. The model also includes the "damaging" and the dissipative channels. The damaging channel is responsible for production of singlet oxygen and other destructive outcomes. In our model, both damaging and "dissipative" charge transfer channels are described by discrete electron energy levels attached to their sinks, that mimic the continuum part of electron energy spectrum. All five excitonic sites interact with the protein environment that is modeled using a stochastic process. Our approach allowed us to derive the exact and closed system of linear ordinary differential equations for the reduced density matrix and its first momentums. These equations are solved numerically including for strong interactions between the light-sensitive molecules and protein environment. As an example, we apply our model to demonstrate possible contributions of quantum interference, protein noise, and sink effects in the NPQ mechanism in the CP29 minor LHC. The numerical simulations show that using proper combination of quantum interference effects, properties of noise, and sinks, one can significantly suppress the damaging channel. Our findings demonstrate the possible role of interference, protein noise, and sink effects for modeling, engineering, and optimizing the performance of the NPQ processes in both natural and artificial light-harvesting complexes.

Natural light harvesting systems: unraveling the quantum puzzles

In natural light harvesting systems, the sequential quantum events of photon absorption by specialized biological antenna complexes, charge separation, exciton formation and energy transfer to localized reaction centers culminates in the conversion of solar to chemical energy. A notable feature in these processes is the exceptionally high efficiencies ( $$>$$ 95 %) at which excitation is transferred from the illuminated protein complex site to the reaction centers. The high speed of excitation propagation within a system of interwoven biomolecular network structures, is yet to be replicated in artificial light harvesting complexes. A clue to unraveling the quantum puzzles of nature may lie in the observations of long lived coherences lasting several picoseconds in the electronic spectra of photosynthetic complexes, which occurs even in noisy environmental baths. However the exact nature of the association between the high energy propagation rates and strength of quantum coherences remains largely unsolved. A number of experimental and theoretical studies have been devoted to unlocking the links between quantum processes and information protocols, in the hope of finding the answers to nature’s puzzling mode of energy propagation. This review presents recent developments in quantum theories, and links information-theoretic aspects with photosynthetic light-harvesting processes in biomolecular systems. There is examination of various attempts to pinpoint the processes that underpin coherence features arising from the light harvesting activities of biomolecular systems, with particular emphasis on the effects that factors such non-Markovianity, zeno mechanisms, teleportation, quantum predictability and the role of multipartite states have on the quantum dynamics of biomolecular systems. A discussion of how quantum thermodynamical principles and agent-based modeling and simulation approaches can improve our understanding of natural photosynthetic systems is included.

Energy transfer in aggregates of bacteriochlorophyll c self-assembled with azulene derivatives

Bacteriochlorophyll (BChl) c is the main light-harvesting pigment of certain photosynthetic bacteria. It is found in the form of self-assembled aggregates in the so-called chlorosomes. Here we report the results of co-aggregation experiments of BChl c with azulene and its tailored derivatives. We have performed spectroscopic and quantum chemical characterization of the azulenes, followed by self-assembly experiments. The results show that only azulenes with sufficient hydrophobicity are able to induce aggregation of BChl c. Interestingly, only azulene derivatives possessing a conjugated phenyl ring were capable of efficient (∼50%) excitation energy transfer to BChl molecules. These aggregates represent an artificial light-harvesting complex with enhanced absorption between 220 and 350 nm compared to aggregates of pure BChl c. The results provide insight into the principles of self-assembly of BChl aggregates and suggest an important role of the π-π interactions in efficient energy transfer.

Wavelet analysis of molecular dynamics: Efficient extraction of time-frequency information in ultrafast optical processes

New experimental techniques based on nonlinear ultrafast spectroscopies have been developed over the last few years, and have been demonstrated to provide powerful probes of quantum dynamics in different types of molecular aggregates, including both natural and artificial light harvesting complexes. Fourier transform-based spectroscopies have been particularly successful, yet "complete" spectral information normally necessitates the loss of all information on the temporal sequence of events in a signal. This information though is particularly important in transient or multi-stage processes, in which the spectral decomposition of the data evolves in time. By going through several examples of ultrafast quantum dynamics, we demonstrate that the use of wavelets provide an efficient and accurate way to simultaneously acquire both temporal and frequency information about a signal, and argue that this greatly aids the elucidation and interpretation of physical process responsible for non-stationary spectroscopic features, such as those encountered in coherent excitonic energy transport.

Coherent optimal control of photosynthetic molecules

We demonstrate theoretically that open-loop quantum optimal control techniques can provide efficient tools for the verification of various quantum coherent transport mechanisms in natural and artificial light-harvesting complexes under realistic experimental conditions. To assess the feasibility of possible biocontrol experiments, we introduce the main settings and derive optimally shaped and robust laser pulses that allow for the faithful preparation of specified initial states (such as localized excitation or coherent superposition, i.e., propagating and nonpropagating states) of the photosystem and probe efficiently the subsequent dynamics. With these tools, different transport pathways can be discriminated, which should facilitate the elucidation of genuine quantum dynamical features of photosystems and therefore enhance our understanding of the role that coherent processes may play in actual biological complexes.

Excitation energy migration in covalently linked perylene bisimide macrocycles

A series of acetylene-linked perylene bisimide (PBI) macrocycles 3a–d with various ring sizes from trimer to hexamer have been synthesised by a palladium-catalysed homocoupling reaction of perylene bisimide 1. Photophysical properties of these PBI macrocycles have been examined by steady-state absorption, fluorescence, fluorescence lifetime, fluorescence anisotropy decay, and transient absorption measurements. Both pump-power dependence on the femtosecond transient absorption and the transient absorption anisotropy decay profiles are directly related with the excitation energy migration processes within PBI macrocycles where the exciton-exciton annihilation time and the polarization anisotropy decay time are well described in terms of the Forster-type incoherent energy hopping model. Consequently, the excitation energy hopping times of macrocycles become slower and then saturated as the ring size increases. Nevertheless, the intrinsically large transition dipole moment of PBI leads to fast energy transfer processes as compared to other artificial light-harvesting complexes such as those constructed from porphyrin building blocks.

Efficient Intrinsic Photoprotection in Strongly Coupled (Bacterio) Chloropyll Complexes

Chlorophyll (Chl) molecules in photosynthetic proteins are known to produce highly toxic singlet oxygen under illumination as a result of energy transfer from their triplet excited states to oxygen. To prevent the formation of singlet oxygen, carotenoids (Car) are typically positioned close to Chl to ensure rapid triplet-triplet energy transfer from Chl to Car, which can then safely dissipate the energy of the excited states. Our recent studies revealed a new, unconventional, but very efficient photoprotection mechanism in strongly coupled natural and artificial light-harvesting complexes that does not rely on the presence of carotenoids. Experimental studies on carotenoid-free chlorosomes and artificial bacteriochlorophyll (BChl) aggregates show that these structures are at least three orders of magnitude more stable to photodamage than monomeric forms of BChl. It was proposed that this photoprotection in strongly coupled arrays of pigments is due to triplet exciton formation, which lowers the energy of the triplet exciton substantially below that of singlet oxygen.In this report we present the results of our ongoing comprehensive study of the properties of triplet excited states of monomeric BChls, Chl aggregates and chlorosomes by means of EPR, time-resolved optical pump-probe spectroscopy and steady-state IR phosphorescence spectroscopy.

Excitation energy transfer in multiporphyrin arrays with cyclic architectures: towards artificial light-harvesting antenna complexes

Since highly symmetric cyclic architecture of light-harvesting antenna complex LH2 in purple bacteria was revealed in 1995, there has been a renaissance in developing cyclic porphyrin arrays to duplicate natural systems in terms of high efficiency, in particular, in transferring excitation energy. This tutorial review highlights the mechanisms and rates of excitation energy transfer (EET) in a variety of synthetic cyclic porphyrin arrays on the basis of time-resolved spectroscopic measurements performed at both ensemble and single-molecule levels. Subtle change in structural parameters such as connectivity, distance, and orientation between neighboring porphyrin moieties exquisitely modulates not only the nature of interchromophoric interactions but also the rates and efficiencies of EET. The relationship between the structure and EET dynamics described here should assist a rational design of novel cyclic porphyrin arrays, more contiguous to real applications in artificial photosynthesis.

Self-assembly and energy transfer in artificial light-harvesting complexes of bacteriochlorophyll c with astaxanthin

Chlorosomes, the light-harvesting antennae of green photosynthetic bacteria, are based on large aggregates of bacteriochlorophyll molecules. Aggregates with similar properties to those in chlorosomes can also be prepared in vitro. Several agents were shown to induce aggregation of bacteriochlorophyll c in aqueous environments, including certain lipids, carotenes, and quinones. A key distinguishing feature of bacteriochlorophyll c aggregates, both in vitro and in chlorosomes, is a large (>60nm) red shift of their Q(y) absorption band compared with that of the monomers. In this study, we investigate the self-assembly of bacteriochlorophyll c with the xanthophyll astaxanthin, which leads to the formation of a new type of complexes. Our results indicate that, due to its specific structure, astaxanthin molecules competes with bacteriochlorophylls for the bonds involved in the aggregation, thus preventing the formation of any significant red shift compared with pure bacteriochlorophyll c in aqueous buffer. A strong interaction between both the types of pigments in the developed assemblies, is manifested by a rather efficient (~40%) excitation energy transfer from astaxanthin to bacteriochlorophyll c, as revealed by fluorescence excitation spectroscopy. Results of transient absorption spectroscopy show that the energy transfer is very fast (<500fs) and proceeds through the S(2) state of astaxanthin.

Optical and Electrical Measurement of Energy Transfer between Nanocrystalline Quantum Dots and Photosystem I

In the natural photosynthesis process, light harvesting complexes (LHCs) absorb light and pass excitation energy to photosystem I (PSI) and photosystem II (PSII). In this study, we have used nanocrystalline quantum dots (NQDs) as an artificial LHC by integrating them with PSI to extend their spectral range. We have performed photoluminescence (PL) and ultrafast time-resolved absorption measurements to investigate this process. Our PL experiments showed that emission from the NQDs is quenched, and the fluorescence from PSI is enhanced. Transient absorption and bleaching results can be explained by fluorescence resonance energy transfer (FRET) from the NQDs to the PSI. This nonradiative energy transfer occurs in ∼6 ps. Current-voltage (I-V) measurements on the composite NQD-PSI samples demonstrate a clear photoresponse.