Photosynthetic Antenna Complexes Research Articles

An integrated approach towards extracting structural characteristics of chlorosomes from a bchQ mutant of Chlorobaculum tepidum.

Chlorosomes, the photosynthetic antenna complexes of green sulfur bacteria, are paradigms for light-harvesting elements in artificial designs, owing to their efficient energy transfer without protein participation. We combined magic angle spinning (MAS) NMR, optical spectroscopy and cryogenic electron microscopy (cryo-EM) to characterize the structure of chlorosomes from a bchQ mutant of Chlorobaculum tepidum. The chlorosomes of this mutant have a more uniform composition of bacteriochlorophyll (BChl) with a predominant homolog, [8Ethyl, 12Ethyl] BChl c, compared to the wild type (WT). Nearly complete 13C chemical shift assignments were obtained from well-resolved homonuclear 13C-13C RFDR data. For proton assignments heteronuclear 13C-1H (hCH) data sets were collected at 1.2 GHz spinning at 60 kHz. The CHHC experiments revealed intermolecular correlations between 132/31, 132/32, and 121/31, with distance constraints of less than 5 Å. These constraints indicate the syn-anti parallel stacking motif for the aggregates. Fourier transform cryo-EM data reveal an axial repeat of 1.49 nm for the helical tubular aggregates, perpendicular to the inter-tube separation of 2.1 nm. This axial repeat is different from WT and is in line with BChl syn-anti stacks running essentially parallel to the tube axis. Such a packing mode is in agreement with the signature of the Qy band in circular dichroism (CD). Combining the experimental data with computational insight suggests that the packing for the light-harvesting function is similar between WT and bchQ, while the chirality within the chlorosomes is modestly but detectably affected by the reduced compositional heterogeneity in bchQ.

Excitation landscape of the CP43 photosynthetic antenna complex from multiscale simulations

QM/MM simulations and the perturbed matrix method are used to investigate a crucial photosynthetic antenna complex, mapping its global excitonic structure and revealing the presence of a low-lying charge transfer state.

Unraveling the role of thermal fluctuations on the exciton structure of the cryptophyte PC612 and PC645 photosynthetic antenna complexes.

Protein scaffolds play a crucial role in tuning the light harvesting properties of photosynthetic pigment-protein complexes, influencing pigment-protein and pigment-pigment excitonic interactions. Here, we investigate the influence of thermal dynamic effects on the protein tuning mechanisms of phycocyanin PC645 and PC612 antenna complexes of cryptophyte algae, featuring closed or open quaternary structures. We employ a dual molecular dynamics (MD) strategy that combines extensive classical MD simulations with multiple short Born-Oppenheimer quantum/molecular mechanical (QM/MM) simulations to accurately account for both static and dynamic disorder effects. Additionally, we compare the results with an alternative protocol based on multiple QM/MM geometry optimizations of the pigments. Subsequently, we employ polarizable QM/MM calculations using time-dependent density functional theory (TD-DFT) to compute the excited states, and we adopt the full cumulant expansion (FCE) formalism to describe the absorption and circular dichroism spectra. Our findings indicate that thermal effects have only minor impacts on the energy ladder in PC612, despite its remarkable flexibility owing to an open quaternary structure. In striking contrast, thermal effects significantly influence the properties of PC645 due to the absence of a hydrogen bond controlling the twist of ring D in PCB β82 bilins, as well as the larger impact of fluctuations on the excited states of MBV pigments, which possess a higher conjugation length compared to other bilin types. Overall, the dual MD protocol combined with the FCE formalism yields excellent spectral properties for PC612 and PC645, and the resultant excitonic Hamiltonians pave the way for future investigations concerning the implications of open and closed quaternary structures on phycocyanin light harvesting properties.

β,β-Directly Linked Porphyrin Rings: Synthesis, Photophysical Properties, and Fullerene Binding.

Cyclic porphyrin oligomers have been studied as models for photosynthetic light-harvesting antenna complexes and as potential receptors for supramolecular chemistry. Here, we report the synthesis of unprecedented β,β-directly linked cyclic zinc porphyrin oligomers, the trimer (CP3) and tetramer (CP4), by Yamamoto coupling of a 2,3-dibromoporphyrin precursor. Their three-dimensional structures were confirmed by nuclear magnetic resonance (NMR) spectroscopy, mass spectrometry, and single-crystal X-ray diffraction analyses. The minimum-energy geometries of CP3 and CP4 have propeller and saddle shapes, respectively, as calculated using density functional theory. Their different geometries result in distinct photophysical and electrochemical properties. The smaller dihedral angles between the porphyrin units in CP3, compared with CP4, result in stronger π-conjugation, splitting the ultraviolet-vis absorption bands and shifting them to longer wavelengths. Analysis of the crystallographic bond lengths indicates that the central benzene ring of the CP3 is partially aromatic [harmonic oscillator model of aromaticity (HOMA) 0.52], whereas the central cyclooctatetraene ring of the CP4 is non-aromatic (HOMA -0.02). The saddle-shaped structure of CP4 makes it a ditopic receptor for fullerenes, with affinity constants of (1.1 ± 0.4) × 105 M-1 for C70 and (2.2 ± 0.1) × 104 M-1 for C60, respectively, in toluene solution at 298 K. The formation of a 1:2 complex with C60 is confirmed by NMR titration and single-crystal X-ray diffraction.

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.

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.

Exciton delocalization in a fully synthetic DNA-templated bacteriochlorin dimer.

A bacteriochlorophyll a (Bchla) dimer is a basic functional unit in the LH1 and LH2 photosynthetic pigment-protein antenna complexes of purple bacteria, where an ordered, close arrangement of Bchla pigments-secured by noncovalent bonding to a protein template-enables exciton delocalization at room temperature. Stable and tunable synthetic analogs of this key photosynthetic subunit could lead to facile engineering of exciton-based systems such as in artificial photosynthesis, organic optoelectronics, and molecular quantum computing. Here, using a combination of synthesis and theory, we demonstrate that exciton delocalization can be achieved in a dimer of a synthetic bacteriochlorin (BC) featuring stability, high structural modularity, and spectral properties advantageous for exciton-based devices. The BC dimer was covalently templated by DNA, a stable and highly programmable scaffold. To achieve exciton delocalization in the absence of pigment-protein interactions critical for the Bchla dimer, we relied on the strong transition dipole moment in BC enabled by two auxochromes along the Qy transition, and omitting the central metal and isocyclic ring. The spectral properties of the synthetic "free" BC closely resembled those of Bchla in an organic solvent. Applying spectroscopic modeling, the exciton delocalization in the DNA-templated BC dimer was evaluated by extracting the excitonic hopping parameter, J to be 214 cm-1 (26.6 meV). For comparison, the same method applied to the natural protein-templated Bchla dimer yielded J of 286 cm-1 (35.5 meV). The smaller value of J in the BC dimer likely arose from the partial bacteriochlorin intercalation and the difference in medium effect between DNA and protein.

Quantum chemical elucidation of a sevenfold symmetric bacterial antenna complex

The light-harvesting complex 2 (LH2) of purple bacteria is one of the most studied photosynthetic antenna complexes. Its symmetric structure and ring-like bacteriochlorophyll arrangement make it an ideal system for theoreticians and spectroscopists. LH2 complexes from most bacterial species are thought to have eightfold or ninefold symmetry, but recently a sevenfold symmetric LH2 structure from the bacterium Mch. purpuratum was solved by Cryo-Electron microscopy. This LH2 also possesses unique near-infrared absorption and circular dichroism (CD) spectral properties. Here we use an atomistic strategy to elucidate the spectral properties of Mch. purpuratum LH2 and understand the differences with the most commonly studied LH2 from Rbl. acidophilus. Our strategy exploits a combination of molecular dynamics simulations, multiscale polarizable quantum mechanics/molecular mechanics calculations, and lineshape simulations. Our calculations reveal that the spectral properties of LH2 complexes are tuned by site energies and exciton couplings, which in turn depend on the structural fluctuations of the bacteriochlorophylls. Our strategy proves effective in reproducing the absorption and CD spectra of the two LH2 complexes, and in uncovering the origin of their differences. This work proves that it is possible to obtain insight into the spectral tuning strategies of purple bacteria by quantitatively simulating the spectral properties of their antenna complexes.

Energy transfer dynamics and the mechanism of biohybrid photosynthetic antenna complexes chemically linked with artificial chromophores.

A light-harvesting strategy is crucial for the utilisation of solar energy. In this study, we addressed the expanding light-harvesting (LH) wavelength of photosynthetic LH complex 2 (LH2, from Rhodoblastus acidophilus strain 10050) through covalent conjugation with extrinsic chromophores. To further understand the conjugation architecture and mechanism of excitation energy transfer (EET), we examined the effects of the linker length and spectral overlap integral between the emission and absorption spectra of the energy donor and acceptor pigments. In the former case, contrary to the intuition based on the Förster resonance energy transfer (FRET) theory, the observed energy transfer rate was similar regardless of the linker length, and the energy transfer efficiency increased with longer linkers. In the latter case, despite the energy transfer rate increases at higher spectral overlaps, it was quantitatively inconsistent with the FRET theory. The mechanism of EET beyond the FRET theory was discussed in terms of the higher-lying exciton state of B850, which mediates efficient EET despite the small spectral overlap. This systematic investigation provides insights for the development of efficient artificial photosynthetic systems.

Production of Carotenoids from Cultivated Seaweed.

Cladosiphon (C.) okamuranus, a brown alga endemic to the Nansei Islands, Japan, has been conventionally ingested as food. Nowadays, it is a major aquatic product of the Okinawa Prefecture with an annual production of around 20,000 tons. The life cycle of C. okamuranus comprises the macroscopic sporophyte (algal body) generation and the microscopic gametophyte generation. The germlings in the latter generation can proliferate when floating in seawater. This floating form has been exploited in techniques involved in the commercial production of C. okamuranus seedlings.Brown algae contain fucoxanthin, a carbonyl carotenoid known to have anticancer, anti-obesity, and antidiabetic effect in addition to the anti-oxidation effect. We found that the fucoxanthin content of cultivated floating form of C. okamuranus discoid germlings becomes up to 50 times that of the mature alga. Since the discoid germlings repeatedly grow like microorganisms, although they are large algae, they are utilized to produce fucoxanthin. We optimize the culture conditions by changing the temperature, light intensity, photoperiod, light wavelength, and nutrient salt conditions for optimal fucoxanthin productivity. The cultivation has been successful to industrial plant scale, culminating in the use of 1 ton of cultivating medium.In brown algal cells, fucoxanthin is primarily found bound to the photosynthetic pigment-protein complexes known as fucoxanthin-chlorophyll protein (FCP). Consequently cultivated floating form of C. okamuranus also shows high content of FCP. Isolation and characterization of pigments bound to the FCP were determined precisely, and ultrafast spectroscopies were applied to elucidate the photosynthetic function of fucoxanthin bound to the pigment-protein complexes. This cultivation method has also been applied to the other edible brown algae. We found that the optimal cultivation conditions as well as the yields of fucoxanthin and FCP highly depend on the species.The floating form cultivation was also applied to a large-sized edible green alga, Codium intricatum, which is uniquely producing a carbonyl carotenoid, siphonaxanthin. This has several anti-disease effects and is also a primal photosynthetic pigment which is found bound to photosynthetic antenna complex usually called siphonaxanthin-chlorophyll protein (SCP). We are working on the improvement of productivity, scale-up of production, and development of cultivation technology of new macro algae.

PHOTOPROTECTIIVE STRATEGIES OF UNICELULAR RED ALGA RHODELLA VIOLACEA DURING ACCLIMATION TO STRONG LIGHT

Red algae contain in their photosynthetic machinery water-soluble antenna complexes - phycobilisomes (PBSs) attached to thylakoid membranes to transfer excitation energy to photosystems. Strong light absorbed by the PBSs triggers a fast formation of transthylakoid ΔpH that follows the non-photochemical quenching of chlorophyll (Chl) fluorescence. The ΔpH build-up seems to be essential for photoprotecting the photosynthetic apparatus in the absence of xanthophyll cycle common to higher plants. However, the photoprotective mechanisms of red algae are not studied in details yet. 
 We present here our research of the Chl fluorescence quenching in unicellular red algae Rhodella violacea and its correlation with the ΔpH gradient being formed. The relation of this phenomenon to photoprotection of photosystem 2 (PS 2) in the normal and high light-acclimated Rhodella cells is also examined. 
 Under the photoinhibitory conditions (white light of 2000-3000 μE/m2s), the ΔpH-dependent Chl fluorescence quenching was found to delay the kinetics of PS 2 photoinhibition. The uncouplers like nigericin and NH4Cl are known to break down ΔpH gradient, lead to the dissipation of Chl fluorescence quenching followed by enhancing the PS 2 photoinhibition rate. The same effect showed far-red (FR) light consuming transthylakoid ΔpH. ATPase inhibitor, DCCD, having no impact on ΔpH didn’t influence PS 2 photoinhibition as well this implies the photoprotection to be fulfilled by the proton gradient rather than by ATP synthesis. 
 Long-term acclimation of Rhodella cells to higher irradiances (500-1000 μE/m2s) results in a partial loss of the periphery phycoerythrin-containing subunits by PBSs. The light-acclimated cultures display a higher resistance to the photoinhibitory light than the non-acclimated ones. This could be explained by diminishing the energy transfer from the reduced PBSs to PS 2 as well as light screening by the secondary carotenoids synthesized during light exposure. 
 Data on low-temperature (77K) fluorescence allow to evaluate the molecular mechanisms of light-induced Chl fluorescence suppression in Rhodella cells and its recovery in darkness.

Salinity impairs photosynthetic capacity and enhances carotenoid-related gene expression and biosynthesis in tomato (Solanum lycopersicum L. cv. Micro-Tom).

Carotenoids are essential components of the photosynthetic antenna and reaction center complexes, being also responsible for antioxidant defense, coloration, and many other functions in multiple plant tissues. In tomato, salinity negatively affects the development of vegetative organs and productivity, but according to previous studies it might also increase fruit color and taste, improving its quality, which is a current agricultural challenge. The fruit quality parameters that are increased by salinity are cultivar-specific and include carotenoid, sugar, and organic acid contents. However, the relationship between vegetative and reproductive organs and response to salinity is still poorly understood. Considering this, Solanum lycopersicum cv. Micro-Tom plants were grown in the absence of salt supplementation as well as with increasing concentrations of NaCl for 14 weeks, evaluating plant performance from vegetative to reproductive stages. In response to salinity, plants showed a significant reduction in net photosynthesis, stomatal conductance, PSII quantum yield, and electron transport rate, in addition to an increase in non-photochemical quenching. In line with these responses the number of tomato clusters decreased, and smaller fruits with higher soluble solids content were obtained. Mature-green fruits also displayed a salt-dependent higher induction in the expression of PSY1, PDS, ZDS, and LYCB, key genes of the carotenoid biosynthesis pathway, in correlation with increased lycopene, lutein, β-carotene, and violaxanthin levels. These results suggest a key relationship between photosynthetic plant response and yield, involving impaired photosynthetic capacity, increased carotenoid-related gene expression, and carotenoid biosynthesis.

Bioinspiration in light harvesting and catalysis

Capturing and converting solar energy into fuels and feedstocks is a global challenge that spans numerous disciplines and fields of research. Billions of years of evolution have allowed natural organisms to hone strategies for harvesting light from the sun and storing energy in the form of carbon–carbon and carbon–hydrogen bonds. Photosynthetic antenna proteins capture solar photons and funnel photoexcitations to reaction centres with high yields, and enzymes catalyze multi-electron reactions, facilitating chemical transformations not yet efficiently implemented using artificially engineered catalysts. Researchers in renewable energy often look to nature to understand the mechanisms at work and, if possible, to explore their translation into artificial systems. Here, we review advances in bioinspiration across the fields of biological light harvesting and chemical energy conversion. We examine how multi-photon and multi-electron reactions in biology can inspire new methods in photoredox chemistry to achieve novel, selective and complex organic transformations; how carbonic-dehydrogenase-inspired design principles enable catalytic reactions such as the conversion of CO2 into useful products such as fuels; and how concepts from photosynthetic antenna complexes and reaction centres can benefit artificial light-harvesting materials. We then consider areas in which bioinspiration could enable advances in the rational design of molecules and materials, the expansion of the synthetic capabilities of catalysts and the valorization of molecular building blocks. We highlight the challenges that must be overcome to realize these advances and propose new directions that may use bioinspiration to achieve them.

Ultrafast Photodynamics and Quantitative Evaluation of Biohybrid Photosynthetic Antenna and Reaction Center Complexes Generating Photocurrent

A functional linkage between light-harvesting and photocatalytic components is a pivotal issue for using solar energy in chemical conversions; however, this concept is far from being practically re...

Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs

Plants prevent photodamage under high light by dissipating excess energy as heat. Conformational changes of the photosynthetic antenna complexes activate dissipation by leveraging the sensitivity of the photophysics to the protein structure. The mechanisms of dissipation remain debated, largely due to two challenges. First, because of the ultrafast timescales and large energy gaps involved, measurements lacked the temporal or spectral requirements. Second, experiments have been performed in detergent, which can induce non-native conformations, or in vivo, where contributions from homologous antenna complexes cannot be disentangled. Here, we overcome both challenges by applying ultrabroadband two-dimensional electronic spectroscopy to the principal antenna complex, LHCII, in a near-native membrane. Our data provide evidence that the membrane enhances two dissipative pathways, one of which is a previously uncharacterized chlorophyll-to-carotenoid energy transfer. Our results highlight the sensitivity of the photophysics to local environment, which may control the balance between light harvesting and dissipation in vivo.

A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection

Carotenoids play a number of important roles in photosynthesis, primarily providing light-harvesting and photoprotective energy dissipation functions within pigment-protein complexes. The carbon-carbon double bond (C=C) conjugation length of carotenoids (N), generally between 9 and 15, determines the carotenoid-to-(bacterio)chlorophyll [(B)Chl] energy transfer efficiency. Here we purified and spectroscopically characterized light-harvesting complex 2 (LH2) from Rhodobacter sphaeroides containing the N = 7 carotenoid zeta (ζ)-carotene, not previously incorporated within a natural antenna complex. Transient absorption and time-resolved fluorescence show that, relative to the lifetime of the S1 state of ζ-carotene in solvent, the lifetime decreases ∼250-fold when ζ-carotene is incorporated within LH2, due to transfer of excitation energy to the B800 and B850 BChls a These measurements show that energy transfer proceeds with an efficiency of ∼100%, primarily via the S1 → Qx route because the S1 → S0 fluorescence emission of ζ-carotene overlaps almost perfectly with the Qx absorption band of the BChls. However, transient absorption measurements performed on microsecond timescales reveal that, unlike the native N ≥ 9 carotenoids normally utilized in light-harvesting complexes, ζ-carotene does not quench excited triplet states of BChl a, likely due to elevation of the ζ-carotene triplet energy state above that of BChl a These findings provide insights into the coevolution of photosynthetic pigments and pigment-protein complexes. We propose that the N ≥ 9 carotenoids found in light-harvesting antenna complexes represent a vital compromise that retains an acceptable level of energy transfer from carotenoids to (B)Chls while allowing acquisition of a new, essential function, namely, photoprotective quenching of harmful (B)Chl triplets.

Spectral Variability in Phycocyanin Cryptophyte Antenna Complexes is Controlled by Changes in the α‐Polypeptide Chains

AbstractQuantitative models of light harvesting in photosynthetic antenna complexes depend sensitively on the challenging determination of the relative site energies of the pigments. Herein we analyze the basis of the light harvesting properties of four antennae from cryptophyte algae, phycocyanines PC577, PC612, PC630 and PC645, by comparing two alternative theoretical strategies to derive the excitonic Hamiltonian. The first is based on molecular dynamics simulations and subsequent polarizable quantum/molecular mechanics (QM/MMPol) calculations, whereas the second is based on three‐layer QM/MMPol/ddCOSMO calculations performed on optimized geometries of the pigments, where the water solvent is described using the ddCOSMO continuum model. We find the latter approach to be remarkably accurate, suggesting that these four phycobiliproteins share a common energetic ordering PCB82 < PCB158 < DBV51/61 for pigments located in the highly‐conserved β chains, whereas bilins in the more divergent α chains cause their spectral differences. In addition, we predict a strong screening of the coupling among central dihydrobiliverdins (DBVs) in “open” form complexes PC577 and PC612 compared to “closed” form ones, which together with the increased interpigment separation explains the attenuation of coherence beatings observed for these complexes.

Neutron and X-ray analysis of the Fenna-Matthews-Olson photosynthetic antenna complex from Prosthecochloris aestuarii.

The Fenna-Matthews-Olson protein from Prosthecochloris aestuarii (PaFMO) has been crystallized in a new form that is amenable to high-resolution X-ray and neutron analysis. The crystals belonged to space group H3, with unit-cell parameters a = b = 83.64, c = 294.78 Å, and diffracted X-rays to ∼1.7 Å resolution at room temperature. Large PaFMO crystals grown to volumes of 0.3-0.5 mm3 diffracted neutrons to 2.2 Å resolution on the MaNDi neutron diffractometer at the Spallation Neutron Source. The resolution of the neutron data will allow direct determination of the positions of H atoms in the structure, which are believed to be fundamentally important in tuning the individual excitation energies of bacteriochlorophylls in this archetypal photosynthetic antenna complex. This is one of the largest unit-cell systems yet studied using neutron diffraction, and will allow the first high-resolution neutron analysis of a photosynthetic antenna complex.

On the existence of superradiant excitonic states in microtubules

Microtubules are biological protein polymers with critical and diverse functions. Their structures share some similarities with photosynthetic antenna complexes, particularly in the ordered arrangement of photoactive molecules with large transition dipole moments. As the role of photoexcitations in microtubules remains an open question, here we analyze tryptophan molecules, the amino acid building block of microtubules with the largest transition dipole strength. By taking their positions and dipole orientations from realistic models capable of reproducing tubulin experimental spectra, and using a Hamiltonian widely employed in quantum optics to describe light–matter interactions, we show that such molecules arranged in their native microtubule configuration exhibit a superradiant lowest exciton state, which represents an excitation fully extended on the chromophore lattice. We also show that such a superradiant state emerges due to supertransfer coupling between the lowest exciton states of smaller blocks of the microtubule. In the dynamics we find that the spreading of excitation is ballistic in the absence of external sources of disorder and strongly dependent on initial conditions. The velocity of photoexcitation spreading is shown to be enhanced by the supertransfer effect with respect to the velocity one would expect from the strength of the nearest-neighbor coupling between tryptophan molecules in the microtubule. Finally, such structures are shown to have an enhanced robustness to static disorder when compared to geometries that include only short-range interactions. These cooperative effects (superradiance and supertransfer) may induce ultra-efficient photoexcitation absorption and could enhance excitonic energy transfer in microtubules over long distances under physiological conditions.

Excitation energy transfer in the far-red absorbing violaxanthin/vaucheriaxanthin chlorophyll a complex from the eustigmatophyte alga FP5.

This work highlights spectroscopic investigations on a new representative of photosynthetic antenna complexes in the LHC family, a putative violaxanthin/vaucheriaxanthin chlorophyll a (VCP) antenna complex from a freshwater Eustigmatophyte alga FP5. A representative VCP-like complex, named as VCP-B3 was studied with both static and time-resolved spectroscopies with the aim of obtaining a deeper understanding of excitation energy migration within the pigment array of the complex. Compared to other VCP representatives, the absorption spectrum of the VCP-B3 is strongly altered in the range of the chlorophyll a Qy band, and is substantially red-shifted with the longest wavelength absorption band at 707nm at 77K. VCP-B3 shows a moderate xanthophyll-to-chlorophyll a efficiency of excitation energy transfer in the 50-60% range, 20-30% lower from comparable VCP complexes from other organisms. Transient absorption studies accompanied by detailed data fitting and simulations support the idea that the xanthophylls that occupy the central part of the complex, complementary to luteins in the LHCII, are violaxanthins. Target analysis suggests that the primary route of xanthophyll-to-chlorophyll a energy transfer occurs via the xanthophyll S1 state.