Light-harvesting Antenna Research Articles

Optical Properties of Concentric Nanorings of Quantum Emitters.

A ring of sub-wavelength spaced dipole-coupled quantum emitters features extraordinary optical properties when compared to a one-dimensional chain or a random collection of emitters. One finds the emergence of extremely subradiant collective eigenmodes similar to an optical resonator, which features strong 3D sub-wavelength field confinement near the ring. Motivated by structures commonly appearing in natural light-harvesting complexes (LHCs), we extend these studies to stacked multi-ring geometries. We predict that using double rings allows us to engineer significantly darker and better confined collective excitations over a broader energy band compared to the single-ring case. These enhance weak field absorption and low-loss excitation energy transport. For the specific geometry of the three rings appearing in the natural LH2 light-harvesting antenna, we show that the coupling between the lower double-ring structure and the higher energy blue-shifted single ring is very close to a critical value for the actual size of the molecule. This creates collective excitations with contributions from all three rings, which is a vital ingredient for efficient and fast coherent inter-ring transport. This geometry thus should also prove useful for the design of sub-wavelength weak field antennae.

Ultrafast Coherent Delocalization Revealed in Multilayer QDs under a Chiral Potential.

In recent years, it was found that current passing through chiral molecules exhibits spin preference, an effect known as Chiral Induced Spin Selectivity (CISS). The effect also enables the reduction of scattering and therefore enhances delocalization. As a result, the delocalization of an exciton generated in the dots is not symmetric and relates to the electronic and hole excited spins. In this work utilizing fast spectroscopy on hybrid multilayered QDs with a chiral polypeptide linker system, we probed the interdot chiral coupling on a short time scale. Surprisingly, we found strong coherent coupling and delocalization despite having long 4-nm chiral linkers. We ascribe the results to asymmetric delocalization that is controlled by the electron spin. The effect is not measured when using shorter nonchiral linkers. As the system mimics light-harvesting antennas, the results may shed light on a mechanism of fast and efficient energy transfer in these systems.

Structure of Dunaliella photosystem II reveals conformational flexibility of stacked and unstacked supercomplexes.

Photosystem II (PSII) generates an oxidant whose redox potential is high enough to enable water oxidation , a substrate so abundant that it assures a practically unlimited electron source for life on earth . Our knowledge on the mechanism of water photooxidation was greatly advanced by high-resolution structures of prokaryotic PSII . Here, we show high-resolution cryogenic electron microscopy (cryo-EM) structures of eukaryotic PSII from the green alga Dunaliella salina at two distinct conformations. The conformers are also present in stacked PSII, exhibiting flexibility that may be relevant to the grana formation in chloroplasts of the green lineage. CP29, one of PSII associated light-harvesting antennae, plays a major role in distinguishing the two conformations of the supercomplex. We also show that the stacked PSII dimer, a form suggested to support the organisation of thylakoid membranes , can appear in many different orientations providing a flexible stacking mechanism for the arrangement of grana stacks in thylakoids. Our findings provide a structural basis for the heterogenous nature of the eukaryotic PSII on multiple levels.

An efficient time-domain implementation of the multichromophoric Förster resonant energy transfer method.

The excitation energy transfer (EET) process for photosynthetic antenna complexes consisting of subunits, each comprised of multiple chromophores, remains challenging to describe. The multichromophoric Förster resonance energy transfer theory is a popular method to describe the EET process in such systems. This paper presents a new time-domain method for calculating energy transfer based on the combination of multichromophoric Förster resonance energy transfer theory and the Numerical Integration of the Schrödinger Equation method. After validating the method on simple model systems, we apply it to the Light-Harvesting antenna 2 (LH2) complex, a light harvesting antenna found in purple bacteria. We use a simple model combining the overdamped Brownian oscillators to describe the dynamic disorder originating from the environmental fluctuations and the transition charge from the electrostatic potential coupling model to determine the interactions between chromophores. We demonstrate that with this model, both the calculated spectra and the EET rates between the two rings within the LH2 complex agree well with experimental results. We further find that the transfer between the strongly coupled rings of neighboring LH2 complexes can also be well described with our method. We conclude that our new method accurately describes the EET rate for biologically relevant multichromophoric systems, which are similar to the LH2 complex. Computationally, the new method is very tractable, especially for slow processes. We foresee that the method can be applied to efficiently calculate transfer in artificial systems as well and may pave the way for calculating multidimensional spectra of extensive multichromophoric systems in the future.

Phycobilisomes and Phycobiliproteins in the Pigment Apparatus of Oxygenic Photosynthetics: From Cyanobacteria to Tertiary Endosymbiosis.

Eukaryotic photosynthesis originated in the course of evolution as a result of the uptake of some unstored cyanobacterium and its transformation to chloroplasts by an ancestral heterotrophic eukaryotic cell. The pigment apparatus of Archaeplastida and other algal phyla that emerged later turned out to be arranged in the same way. Pigment-protein complexes of photosystem I (PS I) and photosystem II (PS II) are characterized by uniform structures, while the light-harvesting antennae have undergone a series of changes. The phycobilisome (PBS) antenna present in cyanobacteria was replaced by Chl a/b- or Chl a/c-containing pigment-protein complexes in most groups of photosynthetics. In the form of PBS or phycobiliprotein aggregates, it was inherited by members of Cyanophyta, Cryptophyta, red algae, and photosynthetic amoebae. Supramolecular organization and architectural modifications of phycobiliprotein antennae in various algal phyla in line with the endosymbiotic theory of chloroplast origin are the subject of this review.

Charge transfer as a mechanism for chlorophyll fluorescence concentration quenching

Highly concentrated solutions of chlorophyll display rapid fluorescence quenching. The same devastating energy loss is not seen in photosynthetic light-harvesting antenna complexes, despite the need for chromophores to be in close proximity to facilitate energy transfer. A promising, though unconfirmed mechanism for the observed quenching is energy transfer from an excited chlorophyll monomer to a closely associated chlorophyll pair that subsequently undergoes rapid nonradiative decay to the ground state via a short-lived intermediate charge-transfer state. In this work, we make use of newly emerging fast methods in quantum chemistry to assess the feasibility of this proposed mechanism. We calculate rate constants for the initial charge separation, based on Marcus free-energy surfaces extracted from molecular dynamics simulations of solvated chlorophyll pairs, demonstrating that this pathway will compete with fluorescence (i.e., drive quenching) at experimentally measured quenching concentrations. We show that the rate of charge separation is highly sensitive to interchlorophyll distance and the relative orientations of chromophores within a quenching pair. We discuss possible solvent effects on the rate of charge separation (and consequently the degree of quenching), using the light-harvesting complex II (LH2) protein from rps. acidophila as a specific example of how this process might be controlled in a protein environment. Crucially, we reveal that the LH2 antenna protein prevents quenching, even at the high chlorophyll concentrations required for efficient energy transfer, by restricting the range of orientations that neighboring chlorophyll pairs can adopt.

Photosynthesis in rice is increased by CRISPR/Cas9-mediated transformation of two truncated light-harvesting antenna.

Plants compete for light partly by over-producing chlorophyll in leaves. The resulting high light absorption is an effective strategy for out competing neighbors in mixed communities, but it prevents light transmission to lower leaves and limits photosynthesis in dense agricultural canopies. We used a CRISPR/Cas9-mediated approach to engineer rice plants with truncated light-harvesting antenna (TLA) via knockout mutations to individual antenna assembly component genes CpSRP43, CpSRP54a, and its paralog, CpSRP54b. We compared the photosynthetic contributions of these components in rice by studying the growth rates of whole plants, quantum yield of photosynthesis, chlorophyll density and distribution, and phenotypic abnormalities. Additionally, we investigated a Poales-specific duplication of CpSRP54. The Poales are an important family that includes staple crops such as rice, wheat, corn, millet, and sorghum. Mutations in any of these three genes involved in antenna assembly decreased chlorophyll content and light absorption and increased photosynthesis per photon absorbed (quantum yield). These results have significant implications for the improvement of high leaf-area-index crop monocultures.

One-helix protein 2 is not required for the synthesis of photosystem II subunit D1 in Chlamydomonas.

In land plants and cyanobacteria, co-translational association of chlorophyll (Chl) to the nascent D1 polypeptide, a reaction center protein of photosystem II (PSII), requires a Chl binding complex consisting of a short-chain dehydrogenase (high chlorophyll fluorescence 244 [HCF244]/uncharacterized protein 39 [Ycf39]) and one-helix proteins (OHP1 and OHP2 in chloroplasts) of the light-harvesting antenna complex superfamily. Here, we show that an ohp2 mutant of the green alga Chlamydomonas (Chlamydomonas reinhardtii) fails to accumulate core PSII subunits, in particular D1 (encoded by the psbA mRNA). Extragenic suppressors arose at high frequency, suggesting the existence of another route for Chl association to PSII. The ohp2 mutant was complemented by the Arabidopsis (Arabidopsis thaliana) ortholog. In contrast to land plants, where psbA translation is prevented in the absence of OHP2, ribosome profiling experiments showed that the Chlamydomonas mutant translates the psbA transcript over its full length. Pulse labeling suggested that D1 is degraded during or immediately after translation. The translation of other PSII subunits was affected by assembly-controlled translational regulation. Proteomics showed that HCF244, a translation factor which associates with and is stabilized by OHP2 in land plants, still partly accumulates in the Chlamydomonas ohp2 mutant, explaining the persistence of psbA translation. Several Chl biosynthesis enzymes overaccumulate in the mutant membranes. Partial inactivation of a D1-degrading protease restored a low level of PSII activity in an ohp2 background, but not photoautotrophy. Taken together, our data suggest that OHP2 is not required for psbA translation in Chlamydomonas, but is necessary for D1 stabilization.

An efficient protocol for excited states of large biochromophores.

Efficient energy transport in photosynthetic antenna is a long-standing source of inspiration for artificial light harvesting materials. However, characterizing the excited states of the constituent chromophores poses a considerable challenge to mainstream quantum chemical and semiempirical excited state methods due to their size and complexity and the accuracy required to describe small but functionally important changes in their properties. In this paper, we explore an alternative approach to calculating the excited states of large biochromophores, exemplified by a specific method for calculating the Qy transition of bacteriochlorophyll a, which we name Chl-xTB. Using a diagonally dominant approximation to the Casida equation and a bespoke parameterization scheme, Chl-xTB can match time-dependent density functional theory's accuracy and semiempirical speed for calculating the potential energy surfaces and absorption spectra of chlorophylls. We demonstrate that Chl-xTB (and other prospective realizations of our protocol) can be integrated into multiscale models, including concurrent excitonic and point-charge embedding frameworks, enabling the analysis of biochromophore networks in a native environment. We exploit this capability to probe the low-frequency spectral densities of excitonic energies and interchromophore interactions in the light harvesting antenna protein LH2 (light harvesting complex 2). The impact of low-frequency protein motion on interchromophore coupling and exciton transport has routinely been ignored due to the prohibitive costs of including it in simulations. Our results provide a more rigorous basis for continued use of this approximation by demonstrating that exciton transition energies are unaffected by low-frequency vibrational coupling to exciton interaction energies.

Mechanism of Absorption Wavelength Shift Depending on the Protonation State of the Acrylate Group in Chlorophyll c.

Diatoms can use light in the blue-green region because they have chlorophyll c (Chlc) in light-harvesting antenna proteins, fucoxanthin and chlorophyll a/c-binding protein (FCP). Chlc has a protonatable acrylate group (-CH═CH-COOH/COO-) conjugated to the porphyrin ring. As the absorption wavelength of Chlc changes upon the protonation of the acrylate group, Chlc is a candidate component that is responsible for photoprotection in diatoms, which switches the FCP function between light-harvesting and energy-dissipation modes depending on the light intensity. Here, we investigate the mechanism by which the absorption wavelength of Chlc changes owing to the change in the protonation state of the acrylate group, using a quantum mechanical/molecular mechanical approach. The calculated absorption wavelength of the Soret band of protonated Chlc is ∼25 nm longer than that of deprotonated Chlc, which is due to the delocalization of the lowest (LUMO) and second lowest (LUMO+1) unoccupied molecular orbitals toward the acrylate group. These results suggest that in FCP, the decrease in pH on the lumenal side under high-light conditions leads to protonation of Chlc and thereby a red shift in the absorption wavelength.

Lab-on-a-DNA origami: nanoengineered single-molecule platforms.

DNA origami nanostructures are self-assembled into almost arbitrary two- and three-dimensional shapes from a long, single-stranded viral scaffold strand and a set of short artificial oligonucleotides. Each DNA strand can be functionalized individually using well-established DNA chemistry, representing addressable sites that allow for the nanometre precise placement of various chemical entities such as proteins, molecular chromophores, nanoparticles, or simply DNA motifs. By means of microscopic and spectroscopic techniques, these entities can be visualized or detected, and either their mutual interaction or their interaction with external stimuli such as radiation can be studied. This gives rise to the Lab-on-a-DNA origami approach, which is introduced in this Feature Article, and the state-of-the-art is summarized with a focus on light-harvesting nanoantennas and DNA platforms for single-molecule analysis either by optical spectroscopy or atomic force microscopy (AFM). Light-harvesting antennas can be generated by the precise arrangement of chromophores to channel and direct excitation energy. At the same time, plasmonic nanoparticles represent a complementary approach to focus light on the nanoscale. Plasmonic nanoantennas also allow for the observation of single molecules either by Raman scattering or fluorescence spectroscopy and DNA origami platforms provide unique opportunities to arrange nanoparticles and molecules to be studied. Finally, the analysis of single DNA motifs by AFM allows for an investigation of radiation-induced processes in DNA with unprecedented detail and accuracy.

Engineering giant excitonic coupling in bioinspired, covalently bridged BODIPY dyads.

Strong excitonic coupling in photosynthetic systems is believed to enable efficient light absorption and quantitative charge separation, motivating the development of artificial multi-chromophore arrays with equally strong or even stronger excitonic coupling. However, large excitonic coupling strengths have typically been accompanied by fast non-radiative recombination, limiting the potential of the arrays for solar energy conversion as well as other applications such as fluorescent labeling. Here, we report giant excitonic coupling leading to broad optical absorption in bioinspired BODIPY dyads that have high photostability, excited-state lifetimes at the nanosecond scale, and fluorescence quantum yields of nearly 50%. Through the synthesis, spectroscopic characterization, and computational modeling of a series of dyads with different linking moieties, we show that the strongest coupling is obtained with diethynylmaleimide linkers, for which the coupling occurs through space between BODIPY units with small separations and slipped co-facial orientations. Other linkers allow for broad tuning of both the relative through-bond and through-space coupling contributions and the overall strength of interpigment coupling, with a tradeoff observed in general between the strength of the two coupling mechanisms. These findings open the door to the synthesis of molecular systems that function effectively as light-harvesting antennas and as electron donors or acceptors for solar energy conversion.

A phototoxic thulium complex exhibiting intracellular ROS production upon 630 nm excitation in cancer cells.

A lanthanide(III) complex with a thulium metal centre connected via a terpyridine unit to a light harvesting antenna with strong absorption in the therapeutic window [>590 nm] was synthesised and tested as a possible photosensitiser (PS) in photodynamic therapy (PDT). The complex exhibited significant phototoxic activity on cancer cells upon irradiation in the therapeutic window and from intracellular and solution studies ROS production was identified as the compound's phototoxic mode of action. In cell viability assays, a 10-fold lowered IC50 value was obtained upon irradiation compared to the dark control.

Reaching strong absorption up to 700 nm with new benzo[g]quinoxaline-based heteroleptic copper(I) complexes for light-harvesting applications.

Heteroleptic copper(I) complexes, with a diimine as a chromophoric unit and a bulky diphosphine as an ancillary ligand, have the advantage of a reduced pseudo Jahn-Teller effect in their excited state over the corresponding homoleptic bis(diimine) complexes. Nevertheless, their lowest absorption lies generally between 350 to 500 nm. Aiming at a strong absorption in the visible by stable heteroleptic Cu(I) complexes, we designed a novel diimine based on 4-(benzo[g]quinoxal-2'-yl)-1,2,3-triazole derivatives. The large π-conjugation of the benzoquinoxaline moiety shifted bathochromically the absorption with regard to other diimine-based Cu(I) complexes. Adding another Cu(I) core broadened the absorption and extended it to considerably longer wavelengths. Moreover, by fine-tuning the structure of the dichelating ligand, we achieved a panchromatic absorption up to 700 nm with a high molar extinction coefficient of 8000 M-1 cm-1 at maximum (λ = 570 nm), making this compound attractive for light-harvesting antennae.

Heteromeric guanosine (G)-quadruplex derived antenna modules with directional energy transfer.

A heteromeric guanosine (G)-quadruplex centered self-assembly approach is developed to prepare compact light-harvesting antenna modules featuring multiple donor dyes and a single toehold region. Due to the mix-and-match nature of our approach, the number and placement of donor dyes can be readily fine-tuned via quadruplex assembly. Moreover, hybridization of the toehold with an acceptor containing sequence results in directional energy transfer ensembles with effective absorption coefficients in the 105 M-1 cm-1 range. These compact antennas exhibit system efficiencies that are comparable to much larger and elaborate DNA architectures containing numerous DNA strands.

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.

Photoinduced NO-release from polymer dots doped with an Ir(III) complex and N-methyl-N-nitroso-4-aminophenol.

Nitric oxide (NO) is a signaling molecule that plays a variety of functions in the human body, but it is difficult to use it in biological experiments or for therapeutic purposes because of its high reactivity and instability in the biological milieu. Consequently, photocontrollable NO releasers, which enable spatiotemporal control of NO release, have an important role in elucidating the functions of NO. Our group has developed visible-light-controllable NO-releasing molecules that contain a fluorescent dye structure as a light-harvesting antenna moiety and an N-nitrosoaminophenol structure as an NO-releasing moiety. Here, we aimed to construct an NO-generating system employing an intermolecular photoredox reaction between the two separate components, since this would simplify chemical synthesis and make it easier to examine various dyes as antennae. For this purpose, we constructed polymer nanoparticles doped with both N-methyl-N-nitroso-4-aminophenol (NAP, 1) and an Ir(III) antenna complex (2, 3 or 4) in order to dissolve in aqueous solution without a co-solvent. These polymer nanoparticles released NO upon photoirradiation in vitro in the purple (400-430 nm) or blue (400-460 nm) wavelength region to activate the doped Ir(III) complex.

Quantification of Photosynthetic Pigments in Neopyropia yezoensis Using Hyperspectral Imagery.

Phycobilisomes and chlorophyll-a (Chla) play important roles in the photosynthetic physiology of red macroalgae and serve as the primary light-harvesting antennae and reaction center for photosystem II. Neopyropia is an economically important red macroalga widely cultivated in East Asian countries. The contents and ratios of 3 main phycobiliproteins and Chla are visible traits to evaluate its commercial quality. The traditional analytical methods used for measuring these components have several limitations. Therefore, a high-throughput, nondestructive, optical method based on hyperspectral imaging technology was developed for phenotyping the pigments phycoerythrin (PE), phycocyanin (PC), allophycocyanin (APC), and Chla in Neopyropia thalli in this study. The average spectra from the region of interest were collected at wavelengths ranging from 400 to 1000 nm using a hyperspectral camera. Following different preprocessing methods, 2 machine learning methods, partial least squares regression (PLSR) and support vector machine regression (SVR), were performed to establish the best prediction models for PE, PC, APC, and Chla contents. The prediction results showed that the PLSR model performed the best for PE (R Test 2 = 0.96, MAPE = 8.31%, RPD = 5.21) and the SVR model performed the best for PC (R Test 2 = 0.94, MAPE = 7.18%, RPD = 4.16) and APC (R Test 2 = 0.84, MAPE = 18.25%, RPD = 2.53). Two models (PLSR and SVR) performed almost the same for Chla (PLSR: R Test 2 = 0.92, MAPE = 12.77%, RPD = 3.61; SVR: R Test 2 = 0.93, MAPE = 13.51%, RPD =3.60). Further validation of the optimal models was performed using field-collected samples, and the result demonstrated satisfactory robustness and accuracy. The distribution of PE, PC, APC, and Chla contents within a thallus was visualized according to the optimal prediction models. The results showed that hyperspectral imaging technology was effective for fast, accurate, and noninvasive phenotyping of the PE, PC, APC, and Chla contents of Neopyropia in situ. This could benefit the efficiency of macroalgae breeding, phenomics research, and other related applications.

Luminescent Silicon Nanowires for Light-Harvesting and Environmental Sensing Applications

Silicon nanowires (Si NWs) represent one of the most promising platforms to be integrated into modern nanodevices. The fabrication of a dense array of vertically aligned ultrathin Si NWs using a low-cost, maskless approach and compatible with Si technology will be here demonstrated. Si NWs with efficient light emission at room temperature (RT) represent a great advance industry, paving the way for a wide range of unexpected photonic applications. In this work I will show the realization of a new hybrid material based on the luminescence of Si NWs and two different dyes for light-harvesting antennas applications, without any surface functionalization and with energy transfer efficiencies higher than 90%. The luminescence of Si NWs has also been used for sensing applications by the realization of highly sensitive sensors for the detecting of low concentrations of toxic gases. These sensors allow the detection of toxic gases below the threshold limits for human health, through both optical and electrical transduction. The achievement of light emission from silicon-based materials represents a revolution in the industrial field, as it paves the way for new Si applications.

Covalently linked pyrene antennas for optically dense yet aggregation-resistant light-harvesting systems.

In this study we present a novel energy transfer material inspired by natural light-harvesting antenna arrays, zinc(II) phthalocyanine-pyrene (ZnPcPy). The ZnPcPy system facilitates energy transfer from 16 covalently linked pyrene (Py) donor chromophores to the emissive central zinc(II) phthalocyanine (ZnPc) core. Nearly 98% energy transfer efficiency is determined from the changes in emission decay rates between free MePy to covalently linked Py, supported by comparisons of photoluminescence quantum yields using different excitation wavelengths. A comparative analysis of ZnPcPy and an equivalent mixture of ZnPc and MePy demonstrates the superior light-harvesting performance of the covalently linked system, with energy transfer rates 9705 times higher in the covalently bound system. This covalent strategy allows for very high loadings of absorbing Py chromophores to be achieved while also avoiding exciton quenching that would otherwise arise, with the same strategy widely applicable to other pairs of Főrster resonance energy transfer (FRET) chromophores.