Phycobilisome's Exciton Transfer Efficiency Relies on an Energetic Funnel Driven by Chromophore-Linker Protein Interactions.

The phycobilisome is the primary light-harvesting antenna in cyanobacterial and red algal oxygenic photosynthesis. It maintains near-unity efficiency of energy transfer to reaction centers despite relying on slow exciton hopping along a relatively sparse network of highly fluorescent phycobilin chromophores. How the complex maintains this high efficiency remains unexplained. Using a two-dimensional electronic spectroscopy polarization scheme that enhances energy transfer features, we directly watch energy flow in the phycobilisome complex of Synechocystis sp. PCC 6803 from the outer phycocyanin rods to the allophycocyanin core. The observed downhill flow of energy, previously hidden within congested spectra, is faster than timescales predicted by Förster hopping along single rod chromophores. We attribute the fast, 8 ps energy transfer to interactions between rod-core linker proteins and terminal rod chromophores, which facilitate unidirectionally downhill energy flow to the core. This mechanism drives the high energy transfer efficiency in the phycobilisome and suggests that linker protein-chromophore interactions have likely evolved to shape its energetic landscape.

2D Nano-Sonosensitizers Facilitate Energy Transfer to Enhance Sonodynamic Therapy.

Although sonodynamic therapy (SDT) has shown promise for cancer treatment, the lack of efficient sonosensitizers (SSs) has limited the clinical application of SDT. Here, a new strategy is reported for designing efficient nano-sonosensitizers based on 2D nanoscale metal-organic layers (MOLs). Composed of Hf-oxo secondary building units (SBUs) and iridium-based linkers, the MOL is anchored with 5,10,15,20-tetra(p-benzoato)porphyrin (TBP) sensitizers on the SBUs to afford TBP@MOL. TBP@MOL shows 14.1- and 7.4-fold higher singlet oxygen (1 O2 ) generation than free TBP ligands and Hf-TBP, a 3D nanoscale metal-organic framework, respectively. The 1 O2 generation of TBP@MOL is enhanced by isolating TBP SSs on the SBUs of the MOL, which prevents aggregation-induced quenching of the excited sensitizers, and by triplet-triplet Dexter energy transfer between excited iridium-based linkers and TBP SSs, which more efficiently harnesses broad-spectrum sonoluminescence. Anchoring TBP on the MOL surface also enhances the energy transfer between the excited sensitizer and ground-state triplet oxygen to increase 1 O2 generation efficacy. In mouse models of colorectal and breast cancer, TBP@MOL demonstrates significantly higher SDT efficacy than Hf-TBP and TBP. This work uncovers a new strategy to design effective nano-sonosensitizers by facilitating energy transfer to efficiently capture broad-spectrum sonoluminescence and enhance 1 O2 generation.

Leveraging Dynamical Symmetries in Two-Dimensional Electronic Spectra to Extract Population Transfer Pathways.

We present a method to deterministically isolate population transfer kinetics from two-dimensional electronic spectroscopic signals. Central to this analysis is the characterization of how all possible subensembles of excited state systems evolve through the population time. When these dynamics are diagrammatically mapped by using double-sided Feynman pathways where population time dynamics are included, a useful symmetry emerges between excited state absorption and ground state bleach recovery dynamics of diagonal and below diagonal cross-peak signals. This symmetry allows removal of pathways from the spectra to isolate signals that evolve according to energy transfer kinetics. We describe a regression procedure to fit to energy transfer time constants and characterize the accuracy of the method in a variety of complex excited state systems using simulated two-dimensional spectra. Our results show that the method is robust for extracting ultrafast energy transfer in multistate excitonic systems, systems containing dark states that affect the signal kinetics, and systems with interfering vibrational relaxation pathways. This procedure can be used to accurately extract energy transfer kinetics from a wide variety of condensed phase systems.

Annihilation of Excess Excitations along Phycocyanin Rods Precedes Downhill Flow to Allophycocyanin Cores in the Phycobilisome of Synechococcus elongatus PCC 7942.

Cyanobacterial phycobilisome complexes absorb visible sunlight and funnel photogenerated excitons to the photosystems where charge separation occurs. In the phycobilisome complex of Synechococcus elongatus PCC 7942, phycocyanin protein rods that absorb bluer wavelengths are assembled on allophycocyanin cores that absorb redder wavelengths. This arrangement creates a natural energy gradient toward the reaction centers of the photosystems. Here, we employ broadband pump-probe spectroscopy to observe the fate of excess excitations in the phycobilisome complex of this organism. We show that excess excitons are quenched through exciton-exciton annihilation along the phycocyanin rods prior to transfer to the allophycocyanin cores. Our observations are especially relevant in comparison to other antenna proteins, where exciton annihilation primarily occurs in the lowest-energy chlorophylls. The observed effect could play a limited photoprotective role in physiological light fluences. The exciton decay dynamics is faster in the intact phycobilisome than in isolated C-phycocyanin trimers studied in earlier work, confirming that this effect is an emergent property of the complex assembly. Using the obtained annihilation data, we calculate exciton hopping times of 2.2-6.4 ps in the phycocyanin rods. This value agrees with earlier FRET calculations of exciton hopping times along phycocyanin hexamers by Sauer and Scheer.

Redox conditions correlated with vibronic coupling modulate quantum beats in photosynthetic pigment-protein complexes.

Quantum coherences, observed as time-dependent beats in ultrafast spectroscopic experiments, arise when light-matter interactions prepare systems in superpositions of states with differing energy and fixed phase across the ensemble. Such coherences have been observed in photosynthetic systems following ultrafast laser excitation, but what these coherences imply about the underlying energy transfer dynamics remains subject to debate. Recent work showed that redox conditions tune vibronic coupling in the Fenna-Matthews-Olson (FMO) pigment-protein complex in green sulfur bacteria, raising the question of whether redox conditions may also affect the long-lived (>100 fs) quantum coherences observed in this complex. In this work, we perform ultrafast two-dimensional electronic spectroscopy measurements on the FMO complex under both oxidizing and reducing conditions. We observe that many excited-state coherences are exclusively present in reducing conditions and are absent or attenuated in oxidizing conditions. Reducing conditions mimic the natural conditions of the complex more closely. Further, the presence of these coherences correlates with the vibronic coupling that produces faster, more efficient energy transfer through the complex under reducing conditions. The growth of coherences across the waiting time and the number of beating frequencies across hundreds of wavenumbers in the power spectra suggest that the beats are excited-state coherences with a mostly vibrational character whose phase relationship is maintained through the energy transfer process. Our results suggest that excitonic energy transfer proceeds through a coherent mechanism in this complex and that the coherences may provide a tool to disentangle coherent relaxation from energy transfer driven by stochastic environmental fluctuations.

Spatial Patterns of Light-Harvesting Antenna Complex Arrangements Tune the Transfer-to-Trap Efficiency of Excitons in Purple Bacteria.

In photosynthesis, the efficiency with which a photogenerated exciton reaches the reaction center is dictated by chromophore energies and the arrangement of chromophores in the supercomplex. Here, we explore the interplay between the arrangement of light-harvesting antennae and the efficiency of exciton transport in purple bacterial photosynthesis. Using a Miller-Abrahams-based exciton hopping model, we compare different arrangements of light-harvesting proteins on the intracytoplasmic membrane. We find that arrangements with aggregated LH1s have a higher efficiency than arrangements with randomly distributed LH1s in a wide range of physiological light fluences. This effect is robust to the introduction of defects on the intracytoplasmic membrane. Our result explains the absence of species with aggregated LH1 arrangements in low-light niches and the large increase seen in the expression of LH1 dimer complexes in high fluences. We suggest that the effect seen in our study is an adaptive strategy toward solar light fluence across different purple bacterial species.

Sub-10 fs Intervalley Exciton Coupling in Monolayer MoS2 Revealed by Helicity-Resolved Two-Dimensional Electronic Spectroscopy.

The valley pseudospin at the K and K' high-symmetry points in monolayer transition metal dichalcogenides (TMDs) has potential as an optically addressable degree of freedom in next-generation optoelectronics. However, intervalley scattering and relaxation of charge carriers leads to valley depolarization and limits practical applications. In addition, enhanced Coulomb interactions lead to pronounced excitonic effects that dominate the optical response and initial valley depolarization dynamics but complicate the interpretation of ultrafast spectroscopic experiments at short time delays. Employing broadband helicity-resolved two-dimensional electronic spectroscopy (2DES), we observe ultrafast (∼10 fs) intervalley coupling between all A and B valley exciton states that results in a complete breakdown of the valley index in large-area monolayer MoS2 films. These couplings and subsequent dynamics exhibit minimal excitation fluence or temperature dependence and are robust toward changes in sample grain size and inherent strain. Our observations strongly suggest that this direct intervalley coupling on the time scale of optical excitation is an inherent property of large-area MoS2 distinct from dynamic carrier or exciton scattering, phonon-driven processes, and multiexciton effects. This ultrafast intervalley coupling poses a fundamental challenge for exciton-based valleytronics in monolayer TMDs and must be overcome to fully realize large-area valleytronic devices.

Photosynthesis tunes quantum-mechanical mixing of electronic and vibrational states to steer exciton energy transfer.

Photosynthetic species evolved to protect their light-harvesting apparatus from photoxidative damage driven by intracellular redox conditions or environmental conditions. The Fenna-Matthews-Olson (FMO) pigment-protein complex from green sulfur bacteria exhibits redox-dependent quenching behavior partially due to two internal cysteine residues. Here, we show evidence that a photosynthetic complex exploits the quantum mechanics of vibronic mixing to activate an oxidative photoprotective mechanism. We use two-dimensional electronic spectroscopy (2DES) to capture energy transfer dynamics in wild-type and cysteine-deficient FMO mutant proteins under both reducing and oxidizing conditions. Under reducing conditions, we find equal energy transfer through the exciton 4-1 and 4-2-1 pathways because the exciton 4-1 energy gap is vibronically coupled with a bacteriochlorophyll-a vibrational mode. Under oxidizing conditions, however, the resonance of the exciton 4-1 energy gap is detuned from the vibrational mode, causing excitons to preferentially steer through the indirect 4-2-1 pathway to increase the likelihood of exciton quenching. We use a Redfield model to show that the complex achieves this effect by tuning the site III energy via the redox state of its internal cysteine residues. This result shows how pigment-protein complexes exploit the quantum mechanics of vibronic coupling to steer energy transfer.

Time-Domain Line-Shape Analysis from 2D Spectroscopy to Precisely Determine Hamiltonian Parameters for a Photosynthetic Complex.

Optical signals come from coherences between quantum states, with spectral line widths determined by the coherences' dephasing dynamics. Using a 2D electronic spectrometer, we observe weak coherence- and rephasing-time-domain signals persisting to 1 ps in the Fenna-Matthews-Olson complex at 77 K. These are coherences between the ground and excited states prepared after the complex interacts once or three times with light, rather than zero-quantum coherences that are more frequently investigated following two interactions. Here, we use these small but persistent signal components to isolate spectral contributions with narrowed peaks and reveal the system's eigenenergies.

Leveraging scatter in two-dimensional spectroscopy: passive phase drift correction enables a global phasing protocol.

Phase stability between pulse pairs defining Fourier-transform time delays can limit resolution and complicates development and adoption of multidimensional coherent spectroscopies. We demonstrate a data processing procedure to correct the long-term phase drift of the nonlinear signal during two-dimensional (2D) experiments based on the relative phase between scattered excitation pulses and a global phasing procedure to generate fully absorptive 2D electronic spectra of wafer-scale monolayer MoS2. Our correction results in a ∼30-fold increase in effective long-term signal phase stability, from ∼λ/2 to ∼λ/70 with negligible extra experimental time and no additional optical components. This scatter-based drift correction should be applicable to other interferometric techniques as well, significantly lowering the practical experimental requirements for this class of measurements.

Ultrafast Excitation Transfer in Cy5 DNA Photonic Wires Displays Dye Conjugation and Excitation Energy Dependency.

DNA scaffolds enable base-pair-specific positioning of fluorescent molecules, allowing for nanometer-scale precision in controlling multidye interactions. Expanding on this concept, DNA-based molecular photonic wires (MPWs) allow for light harvesting and directional propagation of photonic energy on the nanometer scale. The most common MPW examples exploit Förster resonance energy transfer (FRET), and FRET between the same dye species (HomoFRET) was recently shown to increase the distance and efficiency at which MPWs can function. Although increased proximity between adjacent fluorophores can be used to increase the energy transfer efficiency, FRET assumptions break down as the distance between the dye molecules becomes comparable to their size (∼2 nm). Here we compare dye conjugation with single versus dimer Cy5 dye repeats as HomoFRET MPW components on a double-crossover DNA scaffold. At room temperature (RT) under low-light conditions, end-labeled uncoupled dye molecules provide optimal transfer, while the Cy5 dimers show ultrafast (<100 ps) nonradiative decay that severely limits their functionality. Of particular interest is the observation that through increased excitation fluence as well as cryogenic temperatures, the dimeric MPW shows suppression of the ultrafast decay, demonstrating fluorescence lifetimes similar to the single Cy5 MPWs. This work points to the complex dynamic capabilities of dye-based nanophotonic networks, where dye positioning and interactions can become critical, and could be used to extend the lengths and complexities of such dye-DNA devices, enabling multiparameter nanophotonic circuitry.

Evidence for the Dominance of Carrier-Induced Band Gap Renormalization over Biexciton Formation in Cryogenic Ultrafast Experiments on MoS2 Monolayers.

Transition-metal dichalcogenides (TMDs) such as MoS2 display promising electrical and optical properties in the monolayer limit. Due to strong quantum confinement, TMDs provide an ideal environment for exploring excitonic physics using ultrafast spectroscopy. However, the interplay between collective excitation effects on single excitons such as band gap renormalization/exciton binding energy (BGR/EBE) change and multiexciton effects such biexciton formation remains poorly understood. Using two-dimensional electronic spectroscopy, we observe the dominance of single-exciton BGR/EBE signals over optically induced biexciton formation. We make this determination based on a lack of strong PIA features at T = 0 fs in the cryogenic spectra. By means of nodal line slope analysis, we determine that spectral diffusion occurs faster than BGR/EBE change, indicative of distinct processes. These results indicate that at higher sub-Mott limit fluences, collective effects on single excitons dominate biexciton formation.

DNA scaffold supports long-lived vibronic coherence in an indodicarbocyanine (Cy5) dimer.

Vibronic coupling between pigment molecules is believed to prolong coherences in photosynthetic pigment-protein complexes. Reproducing long-lived coherences using vibronically coupled chromophores in synthetic DNA constructs presents a biomimetic route to efficient artificial light harvesting. Here, we present two-dimensional (2D) electronic spectra of one monomeric Cy5 construct and two dimeric Cy5 constructs (0 bp and 1 bp between dyes) on a DNA scaffold and perform beating frequency analysis to interpret observed coherences. Power spectra of quantum beating signals of the dimers reveal high frequency oscillations that correspond to coherences between vibronic exciton states. Beating frequency maps confirm that these oscillations, 1270 cm-1 and 1545 cm-1 for the 0-bp dimer and 1100 cm-1 for the 1-bp dimer, are coherences between vibronic exciton states and that these coherences persist for ∼300 fs. Our observations are well described by a vibronic exciton model, which predicts the excitonic coupling strength in the dimers and the resulting molecular exciton states. The energy spacing between those states closely corresponds to the observed beat frequencies. MD simulations indicate that the dyes in our constructs lie largely internal to the DNA base stacking region, similar to the native design of biological light harvesting complexes. Observed coherences persist on the timescale of photosynthetic energy transfer yielding further parallels to observed biological coherences, establishing DNA as an attractive scaffold for synthetic light harvesting applications.

Orientational Dynamics of Transition Dipoles and Exciton Relaxation in LH2 from Ultrafast Two-Dimensional Anisotropy.

Light-harvesting complexes in photosynthetic organisms display fast and efficient energy transfer dynamics, which depend critically on the electronic structure of the coupled chromophores within the complexes and their interactions with their environment. We present ultrafast anisotropy dynamics, resolved in both time and frequency, of the transmembrane light-harvesting complex LH2 from Rhodobacter sphaeroides in its native membrane environment using polarization-controlled two-dimensional electronic spectroscopy. Time-dependent anisotropy obtained from both experiment and modified Redfield simulation reveals an orientational preference for excited state absorption and an ultrafast equilibration within the B850 band in LH2. This ultrafast equilibration is favorable for subsequent energy transfer toward the reaction center. Our results also show a dynamic difference in excited state absorption anisotropy between the directly excited B850 population and the population that is initially excited at 800 nm, suggesting absorption from B850 states to higher-lying excited states following energy transfer from B850*. These results give insight into the ultrafast dynamics of bacterial light harvesting and the excited state energy landscape of LH2 in the native membrane environment.

Elucidation of near-resonance vibronic coherence lifetimes by nonadiabatic electronic-vibrational state character mixing.

Recent work suggests that the long-lived coherences observed in both natural and artificial light-harvesting systems (such as the Fenna-Matthews-Olson complex) could be attributed to the mixing of the pigments' electronic and vibrational degrees of freedom. To investigate the underlying mechanism of these long coherence lifetimes, a sophisticated description of interactions between the molecular aggregates and the nonequilibrium fluctuations in the surrounding environment is necessary. This is done by implementing the hierarchical equations of motion approach on model homodimers, a method used in the intermediate coupling regime for many molecular aggregates wherein the nonequilibrium environment phonons play nontrivial roles in exciton dynamics. Here we report a character change in the vibronic states-reflective of property mixing between the electronic and vibrational states-induced by an interplay between system coupling parameters within the exciton-vibrational near-resonance regime. This mixing dictates vital aspects of coherence lifetime; by tracking the degree of mixing, we are able to elucidate the relationship between coherence lifetime and both the electronic energy fluctuation and the vibrational relaxation dephasing pathways.

Double-excitation manifold's effect on exciton transfer dynamics and the efficiency of coherent light harvesting.

The efficiency of natural light harvesting systems is largely determined by their ability to transfer excitations from the antenna to the energy trapping center before recombination. The exciton diffusion length similarly limits organic photovoltaics and demands bulk heterojunction architectures. Dark state protection, achieved by coherent coupling between subunits within the antenna, can significantly reduce radiative recombination and enhance the efficiency of energy trapping. In this work we extend the dark state concept to the double-excitation manifold by studying the dynamical flow of excitations. We show that the lowest double-excitation state carries minimal oscillator strength, but relaxation to this state from higher lying double excitations can be relatively rapid such that the lowest double excitation state can act as a dynamical dark state protecting excitation from radiative recombination. This mechanism is sensitive to topology and operates differently for chain and ring structures, while becoming more pronounced in both geometries when the size of the antenna increases. When the exciton-exciton annihilation (EEA) mechanism is considered, the double-excitation population is quickly depleted and the dynamics change dramatically. However the efficiency and output power are still significantly different from those calculated using the single-excitation manifold alone, justifying the necessity of considering the double-excitation manifold. Remarkably, in certain scenarios, EEA can even increase the overall light harvesting efficiency by bringing population down from the double-excitation dark states to the single-excitation manifold.

Origin of Broad Emission Spectra in InP Quantum Dots: Contributions from Structural and Electronic Disorder.

The ensemble emission spectra of colloidal InP quantum dots are broader than achievable spectra of cadmium- and lead-based quantum dots, despite similar single-particle line widths and significant efforts invested in the improvement of synthetic protocols. We seek to explain the origin of persistently broad ensemble emission spectra of colloidal InP quantum dots by investigating the nature of the electronic states responsible for luminescence. We identify a correlation between red-shifted emission spectra and anomalous broadening of the excitation spectra of luminescent InP colloids, suggesting a trap-associated emission pathway in highly emissive core-shell quantum dots. Time-resolved pump-probe experiments find that electrons are largely untrapped on photoluminescence relevant time scales pointing to emission from recombination of localized holes with free electrons. Two-dimensional electronic spectroscopy on InP quantum dots reveals multiple emissive states and increased electron-phonon coupling associated with hole localization. These localized hole states near the valence band edge are hypothesized to arise from incomplete surface passivation and structural disorder associated with lattice defects. We confirm the presence and effect of lattice disorder by X-ray absorption spectroscopy and Raman scattering measurements. Participation of localized electronic states that are associated with various classes of lattice defects gives rise to phonon-coupled defect related emission. These findings explain the origins of the persistently broad emission spectra of colloidal InP quantum dots and suggest future strategies to narrow ensemble emission lines comparable to what is observed for cadmium-based materials.

Connecting bright and dark states through accidental degeneracy caused by lack of symmetry.

Coupled excitonic structures are found in natural and artificial light harvesting systems where optical transitions link different excitation manifolds. In systems with symmetry, some optical transitions are allowed, while others are forbidden. Here we examine an excitonic ring structure and identify an accidental degeneracy between two categories of double-excitation eigenstates with distinct symmetries and optical transition properties. To understand the accidental degeneracy, a complete selection rule between two arbitrary excitation manifolds is derived with a physically motivated proof. Remarkably, symmetry analysis shows that the lack of certain symmetry elements in the Hamiltonian is responsible for this degeneracy, which is unique to rings with size N = 4l + 2 (l being an integer).

Disentanglement of excited-state dynamics with implications for FRET measurements: two-dimensional electronic spectroscopy of a BODIPY-functionalized cavitand.

Förster Resonance Energy Transfer (FRET) is the incoherent transfer of an electronic excitation from a donor fluorophore to a nearby acceptor. FRET has been applied as a probe of local chromophore environments and distances on the nanoscale by extrapolating transfer efficiencies from standard experimental parameters, such as fluorescence intensities or lifetimes. Competition from nonradiative relaxation processes is often assumed to be constant in these extrapolations, but in actuality, this competition depends on the donor and acceptor environments and can, therefore, be affected by conformational changes. To study the effects of nonradiative relaxation on FRET dynamics, we perform two-dimensional electronic spectroscopy (2DES) on a pair of azaboraindacene (BODIPY) dyes, attached to opposite arms of a resorcin[4]arene cavitand. Temperature-induced switching between two equilibrium conformations, vase at 294 K to kite at 193 K, increases the donor-acceptor distance from 0.5 nm to 3 nm, affecting both FRET efficiency and nonradiative relaxation. By disentangling different dynamics based on lifetimes extracted from a series of 2D spectra, we independently observe nonradiative relaxation, FRET, and residual fluorescence from the donor in both vase to kite conformations. We observe changes in both FRET rate and nonradiative relaxation when the molecule switches from vase to kite, and measure a significantly greater difference in transfer efficiency between conformations than would be determined by standard lifetime-based measurements. These observations show that changes in competing nonradiative processes must be taken into account when highly accurate measurements of FRET efficiency are desired.

Crystal structure of 4'-allyl-4,5,6,7,2',7'-hexa-chloro-fluorescein allyl ester unknown solvate.

In the title compound, 4'-allyl-4,5,6,7,2',7'-hexa-chloro-fluorescein allyl ester {systematic name: prop-2-en-1-yl 2,3,4,5-tetra-chloro-6-[2,7-di-chloro-6-hy-droxy-3-oxo-4-(prop-2-en-1-yl)-3H-xanthen-9-yl]benzoate}, C26H14Cl6O5, accompanied by unknown solvate molecules, the dihedral angle between the xanthene ring system (r.m.s. deviation = 0.046 Å) and the penta-substituted benzene ring is 71.67 (9)°. Both allyl groups are disordered over two sets of sites in statistical ratios. The scattering contributions of the disordered solvent mol-ecules (both Ph2O and CHCl3, as identified by NMR) were removed with the PLATON SQUEEZE algorithm [Spek (2015 ▸). Acta Cryst. C71, 9-18]. In the crystal, tetra-meric supra-molecular aggregates linked by O-H⋯O hydrogen bonds occur; these further inter-act with neighboring aggregates through C-Cl⋯π inter-actions arising from the benzene rings, forming infinite two-dimensional sheets. Each C6Cl4 ring shifts in the direction perpendicular to the two-dimensional sheet, exhibiting a helical chain in which every C6Cl4 ring is utilized as both a donor and an acceptor of Cl⋯π contacts. Thus, these two-dimensional sheets pack in a helical fashion, constructing a three-dimensional network.