Fundamental limits on wavelength, efficiency and yield of the charge separation triad.
ABSTRACT: In an attempt to optimize a high yield, high efficiency artificial photosynthetic protein we have discovered unique energy and spatial architecture limits which apply to all light-activated photosynthetic systems. We have generated an analytical solution for the time behavior of the core three cofactor charge separation element in photosynthesis, the photosynthetic cofactor triad, and explored the functional consequences of its makeup including its architecture, the reduction potentials of its components, and the absorption energy of the light absorbing primary-donor cofactor. Our primary findings are two: First, that a high efficiency, high yield triad will have an absorption frequency more than twice the reorganization energy of the first electron transfer, and second, that the relative distance of the acceptor and the donor from the primary-donor plays an important role in determining the yields, with the highest efficiency, highest yield architecture having the light absorbing cofactor closest to the acceptor. Surprisingly, despite the increased complexity found in natural solar energy conversion proteins, we find that the construction of this central triad in natural systems matches these predictions. Our analysis thus not only suggests explanations for some aspects of the makeup of natural photosynthetic systems, it also provides specific design criteria necessary to create high efficiency, high yield artificial protein-based triads.
Project description:Förster’s theory of resonant energy transfer underlies a fundamental process in nature, namely the harvesting of sunlight by photosynthetic life forms. The theoretical framework developed by Förster and others describes how electronic excitation migrates in the photosynthetic apparatus of plants, algae, and bacteria from light absorbing pigments to reaction centers where light energy is utilized for the eventual conversion into chemical energy. The demand for highest possible efficiency of light harvesting appears to have shaped the evolution of photosynthetic species from bacteria to plants which, despite a great variation in architecture, display common structural themes founded on the quantum physics of energy transfer as described first by Förster. Herein, Förster’s theory of excitation transfer is summarized, including recent extensions, and the relevance of the theory to photosynthetic systems as evolved in purple bacteria, cyanobacteria, and plants is demonstrated. Förster’s energy transfer formula, as used widely today in many fields of science, is also derived.
Project description:In the photosynthetic photosystem II, electrons are transferred from the manganese-containing oxygen evolving complex (OEC) to the oxidized primary electron-donor chlorophyll P680(•+) by a proton-coupled electron transfer process involving a tyrosine-histidine pair. Proton transfer from the tyrosine phenolic group to a histidine nitrogen positions the redox potential of the tyrosine between those of P680(•+) and the OEC. We report the synthesis and time-resolved spectroscopic study of a molecular triad that models this electron transfer. The triad consists of a high-potential porphyrin bearing two pentafluorophenyl groups (PF(10)), a tetracyanoporphyrin electron acceptor (TCNP), and a benzimidazole-phenol secondary electron-donor (Bi-PhOH). Excitation of PF(10) in benzonitrile is followed by singlet energy transfer to TCNP (? = 41 ps), whose excited state decays by photoinduced electron transfer (? = 830 ps) to yield Bi-PhOH-PF(10)(•+)-TCNP(•-). A second electron transfer reaction follows (? < 12 ps), giving a final state postulated as BiH(+)-PhO(•)-PF(10)-TCNP(•-), in which the phenolic proton now resides on benzimidazole. This final state decays with a time constant of 3.8 ?s. The triad thus functionally mimics the electron transfers involving the tyrosine-histidine pair in PSII. The final charge-separated state is thermodynamically capable of water oxidation, and its long lifetime suggests the possibility of coupling systems such as this system to water oxidation catalysts for use in artificial photosynthetic fuel production.
Project description:Photosystem I coordinates more than 90 chlorophylls in its core antenna while achieving near perfect quantum efficiency. Low energy chlorophylls (also known as red chlorophylls) residing in the antenna are important for energy transfer dynamics and yield, however, their precise location remained elusive. Here, we construct a chimeric Photosystem I complex in Synechocystis PCC 6803 that shows enhanced absorption in the red spectral region. We combine Cryo-EM and spectroscopy to determine the structure-function relationship in this red-shifted Photosystem I complex. Determining the structure of this complex reveals the precise architecture of the low energy site as well as large scale structural heterogeneity which is probably universal to all trimeric Photosystem I complexes. Identifying the structural elements that constitute red sites can expand the absorption spectrum of oxygenic photosynthetic and potentially modulate light harvesting efficiency.
Project description:High temperature and high light intensity is a common environment posing a great risk to organisms. This study aimed to elucidate the effects of sub-high temperature and high light intensity stress (HH, 35°C, 1000 ?mol?m-2?s-1) and recovery on the photosynthetic mechanism, photoinhibiton of photosystem II (PSII) and photosystem I (PSI), and reactive oxygen (ROS) metabolism of tomato seedlings. The results showed that with prolonged stress time, net photosynthetic rate (Pn), Rubisco activity, maximal photochemistry efficiency (Fv/Fm), efficient quantum yield and electron transport of PSII [Y(II) and ETR(II)] and PSI [Y(I) and ETR(I)] decreased significantly whereas yield of non-regulated and regulated energy dissipation of PSII [Y(NO) and Y(NPQ)] increased sharply. The donor side limitation of PSI [Y(ND)] increased but the acceptor side limitation of PSI [Y(NA)] decreased. Content of malondialdehyde (MDA) and hydrogen peroxide (H2O2) were increased while activity of superoxide dismutase (SOD) and peroxidase (POD) were significantly inhibited compared with control. HH exposure affected photosynthetic carbon assimilation, multiple sites in PSII and PSI, ROS accumulation and elimination of Solanum lycopersicum L.
Project description:Crop canopies create environments of highly fluctuating light intensities. In such environments, photoprotective mechanisms and their relaxation kinetics have been hypothesized to limit photosynthetic efficiency and therefore crop yield potential. Here, we show that overexpression of the Arabidopsis thylakoid K+/H+ antiporter KEA3 accelerates the relaxation of photoprotective energy-dependent quenching after transitions from high to low light in Arabidopsis and tobacco. This, in turn, enhances PSII quantum efficiency in both organisms, supporting that in wild-type plants, residual light energy quenching following a high to low light transition represents a limitation to photosynthetic efficiency in fluctuating light. This finding underscores the potential of accelerating quenching relaxation as a building block for improving photosynthetic efficiency in the field. Additionally, by overexpressing natural KEA3 variants with modification to the C-terminus, we show that KEA3 activity is regulated by a mechanism involving its lumen-localized C-terminus, which lowers KEA3 activity in high light. This regulatory mechanism fine-tunes the balance between photoprotective energy dissipation in high light and maximum quantum yield in low light, likely to be critical for efficient photosynthesis in fluctuating light conditions.
Project description:Low light (LL) is one of the main limiting factors that negatively affect tomato growth and yield. Techniques of chemical regulation are effective horticultural methods to improve stress resistance. Strigolactones (SLs), newly discovered phytohormones, are considered as important regulators of physiological responses. We investigated the effects of foliage spray of GR24, a synthesized SLs, on tomato seedlings grown under LL stress conditions. The results showed that application of GR24 effectively mitigated the inhibition of plant growth and increased the fresh and dry weight of tomato plants under LL. Additionally, GR24 also increased the chlorophyll content (Chla and Chlb), the net photosynthetic rate (Pn), the photochemical efficiency of photosystem (PS) II (Fv/Fm), and the effective quantum yield of PSII and I [Y(II) and Y(I)], but decreased the excitation pressure of PSII (1-qP), the non-regulatory quantum yield of energy dissipation [Y(NO)] and the donor side limitation of PSI [Y(ND)] under LL. Moreover, application of GR24 to LL-stressed tomato leaves increased the electron transport rate of PSII and PSI [ETR(II) and ETR(I)], the ratio of the quantum yield of cyclic electron flow (CEF) to Y(II) [Y(CEF)/Y(II)], the oxidized plastoquinone (PQ) pool size and the non-photochemical quenching. Besides, GR24 application increased the activity and gene expression of antioxidant enzymes, but it reduced malonaldehyde (MDA) and hydrogen peroxide (H2O2) content in LL-stressed plants. These results suggest that exogenous application of GR24 enhances plant tolerance to LL by promoting plant utilization of light energy to alleviate the photosystem injuries induced by excess light energy and ROS, and enhancing photosynthesis efficiency to improve plant growth.
Project description:Surface plasmon (SP) coupling has been successfully applied to nonradiative energy transfer via exciton-plasmon-exciton coupling in conventionally sandwiched donor-metal film-acceptor configurations. However, these structures lack the desired efficiency and suffer poor photoemission due to the high energy loss. Here, we show that the cascaded exciton-plasmon-plasmon-exciton coupling in stratified architecture enables an efficient energy transfer mechanism. The overlaps of the surface plasmon modes at the metal-dielectric and dielectric-metal interfaces allow for strong cross-coupling in comparison with the single metal film configuration. The proposed architecture has been demonstrated through the analytical modeling and numerical simulation of an oscillating dipole near the stratified nanostructure of metal-dielectric-metal-acceptor. Consistent with theoretical and numerical results, experimental measurements confirm at least 50% plasmon resonance energy transfer enhancement in the donor-metal-dielectric-metal-acceptor compared to the donor-metal-acceptor structure. Cascaded plasmon-plasmon coupling enables record high efficiency for exciton transfer through metallic structures.
Project description:Background Leaf size and shape, which affect light capture, and chlorophyll content are important factors affecting photosynthetic efficiency. Genetic variation of these components significantly affects yield potential and seed quality. Identification of the genetic basis for these traits and the relationship between them is of great practical significance for achieving ideal plant architecture and high photosynthetic efficiency for improved yield. Results Here, we undertook a large-scale linkage mapping study using three mapping populations to determine the genetic interplay between soybean leaf-related traits and chlorophyll content across two environments. Correlation analysis revealed a significant negative correlation between leaf size and shape, while both traits were positively correlated with chlorophyll content. This phenotypic relationship was verified across the three mapping populations as determined by principal component analysis, suggesting that these traits are under the control of complex and interrelated genetic components. The QTLs for leaf-related traits and chlorophyll are partly shared, which further supports the close genetic relationship between the two traits. The largest-effect major loci, q20, was stably identified across all population and environments and harbored the narrow leaflet gene Gm-JAG1 (Ln/ln), which is a key regulator of leaflet shape in soybean. Conclusion Our results uncover several major QTLs (q4–1, q4–2, q11, q13, q18 and q20) and its candidate genes specific or common to leaf-related traits and chlorophyll, and also show a complex epistatic interaction between the two traits. The SNP markers closely linked to these valuable QTLs could be used for molecular design breeding with improved plant architecture, photosynthetic capacity and even yield.
Project description:Two seemingly unrelated effects attributed to quantum coherence have been reported recently in natural and artificial light-harvesting systems. First, an enhanced solar cell efficiency was predicted and second, population oscillations were measured in photosynthetic antennae excited by sequences of coherent ultrashort laser pulses. Because both systems operate as quantum heat engines (QHEs) that convert the solar photon energy to useful work (electric currents or chemical energy, respectively), the question arises whether coherence could also enhance the photosynthetic yield. Here, we show that both effects arise from the same population-coherence coupling term which is induced by noise, does not require coherent light, and will therefore work for incoherent excitation under natural conditions of solar excitation. Charge separation in light-harvesting complexes occurs in a pair of tightly coupled chlorophylls (the special pair) at the heart of photosynthetic reaction centers of both plants and bacteria. We show the analogy between the energy level schemes of the special pair and of the laser/photocell QHEs, and that both population oscillations and enhanced yield have a common origin and are expected to coexist for typical parameters. We predict an enhanced yield of 27% in a QHE motivated by the reaction center. This suggests nature-mimicking architectures for artificial solar energy devices.
Project description:Photosynthetic reaction centers convert light energy into chemical energy in a series of transmembrane electron transfer reactions, each with near 100% yield. The structures of reaction centers reveal two symmetry-related branches of cofactors (denoted A and B) that are functionally asymmetric; purple bacterial reaction centers use the A pathway exclusively. Previously, site-specific mutagenesis has yielded reaction centers capable of transmembrane charge separation solely via the B branch cofactors, but the best overall electron transfer yields are still low. In an attempt to better realize the architectural and energetic factors that underlie the directionality and yields of electron transfer, sites within the protein-cofactor complex were targeted in a directed molecular evolution strategy that implements streamlined mutagenesis and high throughput spectroscopic screening. The polycistronic approach enables efficient construction and expression of a large number of variants of a heteroligomeric complex that has two intimately regulated subunits with high sequence similarity, common features of many prokaryotic and eukaryotic transmembrane protein assemblies. The strategy has succeeded in the discovery of several mutant reaction centers with increased efficiency of the B pathway; they carry multiple substitutions that have not been explored or linked using traditional approaches. This work expands our understanding of the structure-function relationships that dictate the efficiency of biological energy-conversion reactions, concepts that will aid the design of bio-inspired assemblies capable of both efficient charge separation and charge stabilization.