Elucidating interprotein energy transfer dynamics within the antenna network from purple bacteria.

In photosynthesis, absorbed light energy transfers through a network of antenna proteins with near-unity quantum efficiency to reach the reaction center, which initiates the downstream biochemical reactions. While the energy transfer dynamics within individual antenna proteins have been extensively studied over the past decades, the dynamics between the proteins are poorly understood due to the heterogeneous organization of the network. Previously reported timescales averaged over such heterogeneity, obscuring individual interprotein energy transfer steps. Here, we isolated and interrogated interprotein energy transfer by embedding two variants of the primary antenna protein from purple bacteria, light-harvesting complex 2 (LH2), together into a near-native membrane disc, known as a nanodisc. We integrated ultrafast transient absorption spectroscopy, quantum dynamics simulations, and cryogenic electron microscopy to determine interprotein energy transfer timescales. By varying the diameter of the nanodiscs, we replicated a range of distances between the proteins. The closest distance possible between neighboring LH2, which is the most common in native membranes, is 25 Šand resulted in a timescale of 5.7 ps. Larger distances of 28 to 31 Šresulted in timescales of 10 to 14 ps. Corresponding simulations showed that the fast energy transfer steps between closely spaced LH2 increase transport distances by ∼15%. Overall, our results introduce a framework for well-controlled studies of interprotein energy transfer dynamics and suggest that protein pairs serve as the primary pathway for the efficient transport of solar energy.

Engineering Exciton Dynamics with Synthetic DNA Scaffolds.

Excitons are the molecular-scale currency of electronic energy. Control over excitons enables energy to be directed and harnessed for light harvesting, electronics, and sensing. Excitonic circuits achieve such control by arranging electronically active molecules to prescribe desired spatiotemporal dynamics. Photosynthetic solar energy conversion is a canonical example of the power of excitonic circuits, where chromophores are positioned in a protein scaffold to perform efficient light capture, energy transport, and charge separation. Synthetic systems that aim to emulate this functionality include self-assembled aggregates, molecular crystals, and chromophore-modified proteins. While the potential of this approach is clear, these systems lack the structural precision to control excitons or even test the limits of their power. In recent years, DNA origami has emerged as a designer material that exploits biological building blocks to construct nanoscale architectures. The structural precision afforded by DNA origami has enabled the pursuit of naturally inspired organizational principles in a highly precise and scalable manner. In this Account, we describe recent developments in DNA-based platforms that spatially organize chromophores to construct tunable excitonic systems. The high fidelity of DNA base pairing enables the formation of programmable nanoscale architectures, and sequence-specific placement allows for the precise positioning of chromophores within the DNA structure. The integration of a wide range of chromophores across the visible spectrum introduces spectral tunability. These excitonic DNA-chromophore assemblies not only serve as model systems for light harvesting, solar conversion, and sensing but also lay the groundwork for the integration of coupled chromophores into larger-scale nucleic acid architectures.We have used this approach to generate DNA-chromophore assemblies of strongly coupled delocalized excited states through both sequence-specific self-assembly and the covalent attachment of chromophores. These strategies have been leveraged to independently control excitonic coupling and system-bath interaction, which together control energy transfer. We then extended this framework to identify how scaffold configurations can steer the formation of symmetry-breaking charge transfer states, paving the way toward the design of dual light-harvesting and charge separation DNA machinery. In an orthogonal application, we used the programmability of DNA chromophore assemblies to change the optical emission properties of strongly coupled dimers, generating a series of fluorophore-modified constructs with separable emission properties for fluorescence assays. Upcoming advances in the chemical modification of nucleotides, design of large-scale DNA origami, and predictive computational methods will aid in constructing excitonic assemblies for optical and computing applications. Collectively, the development of DNA-chromophore assemblies as a platform for excitonic circuitry offers a pathway to identifying and applying design principles for light harvesting and molecular electronics.

Peer support during in vivo exposure homework increases likelihood of prolonged exposure therapy completion.

Exposure-based treatments such as prolonged exposure therapy (PE) are effective for veterans with PTSD. However, dropout rates as high as 50% are common. The Department of Veterans Affairs employs peers to increase mental health treatment engagement, however peers are not routinely used to help patients complete PE homework assignments. The present study included 109 veterans who decided to drop out from exposure-based treatment after completing seven or fewer sessions and used a randomized controlled design to compare PE treatment completion rates in response to 2 forms of peer support: (1) standard weekly telephone-based peer support vs. (2) peer-assisted in vivo exposure, wherein peers accompanied veterans (virtually or in person) during a limited number of in vivo exposure assignments. There were no differences between instrumental vs general peer support conditions as randomized. However, post hoc analyses indicated that 87% of those who completed at least one peer-assisted in vivo exposure completed treatment, compared to 56% of those not completing any peer-assisted in vivo exposure. The dose effect of peer-assisted in vivo exposure increased to 93% with 2 or more peer-assisted exposures, and 97% with 3 or more peer-assisted exposures. The present study suggests that augmenting PE with instrumental peer support during in vivo exposure homework may reduce dropout if completed. Future research should test whether the impact of peer-assisted in vivo exposure is enhanced when offered at the beginning of treatment as opposed to waiting until the point of dropout.

Sculpting photoproducts with DNA origami.

Natural light-harvesting systems spatially organize densely packed dyes in different configurations to either transport excitons or convert them into charge photoproducts, with high efficiency. In contrast, artificial photosystems like organic solar cells and light-emitting diodes lack this fine structural control, limiting their efficiency. Thus, biomimetic multi-dye systems are needed to organize dyes with the sub-nanometer spatial control required to sculpt resulting photoproducts. Here, we synthesize 11 distinct perylene diimide (PDI) dimers integrated into DNA origami nanostructures and identify dimer architectures that offer discrete control over exciton transport versus charge separation. The large structural-space and site-tunability of origami uniquely provides controlled PDI dimer packing to form distinct excimer photoproducts, which are sensitive to interdye configurations. In the future, this platform enables large-scale programmed assembly of dyes mimicking natural systems to sculpt distinct photophysical products needed for a broad range of optoelectronic devices, including solar energy converters and quantum information processors.

Observation of parallel intersystem crossing and charge transfer-state dynamics in [Fe(bpy)3]2+ from ultrafast 2D electronic spectroscopy.

Transition metal-based charge-transfer complexes represent a broad class of inorganic compounds with diverse photochemical applications. Charge-transfer complexes based on earth-abundant elements have been of increasing interest, particularly the canonical [Fe(bpy)3]2+. Photoexcitation into the singlet metal-ligand charge transfer (1MLCT) state is followed by relaxation first to the ligand-field manifold and then to the ground state. While these dynamics have been well-studied, processes within the MLCT manifold that facilitate and/or compete with relaxation have been more elusive. We applied ultrafast two-dimensional electronic spectroscopy (2DES) to disentangle the dynamics immediately following MLCT excitation of this compound. First, dynamics ascribed to relaxation out of the initially formed 1MLCT state was found to correlate with the inertial response time of the solvent. Second, the additional dimension of the 2D spectra revealed a peak consistent with a ∼20 fs 1MLCT → 3MLCT intersystem crossing process. These two observations indicate that the complex simultaneously undergoes intersystem crossing and direct conversion to ligand-field state(s). Resolution of these parallel pathways in this prototypical earth-abundant complex highlights the ability of 2DES to deconvolve the otherwise obscured excited-state dynamics of charge-transfer complexes.

Tuning Optical Absorption and Emission Using Strongly Coupled Dimers in Programmable DNA Scaffolds.

Molecular materials for light harvesting, computing, and fluorescence imaging require nanoscale integration of electronically active subunits. Variation in the optical absorption and emission properties of the subunits has primarily been achieved through modifications to the chemical structure, which is often synthetically challenging. Here, we introduce a facile method for varying optical absorption and emission properties by changing the geometry of a strongly coupled Cy3 dimer on a double-crossover (DX) DNA tile. Leveraging the versatility and programmability of DNA, we tune the length of the complementary strand so that it "pushes" or "pulls" the dimer, inducing dramatic changes in the photophysics including lifetime differences observable at the ensemble and single-molecule level. The separable lifetimes, along with environmental sensitivity also observed in the photophysics, suggest that the Cy3-DX tile constructs could serve as fluorescence probes for multiplexed imaging. More generally, these constructs establish a framework for easily controllable photophysics via geometric changes to coupled chromophores, which could be applied in light-harvesting devices and molecular electronics.

Activating charge-transfer state formation in strongly-coupled dimers using DNA scaffolds.

Strongly-coupled multichromophoric assemblies orchestrate the absorption, transport, and conversion of photonic energy in natural and synthetic systems. Programming these functionalities involves the production of materials in which chromophore placement is precisely controlled. DNA nanomaterials have emerged as a programmable scaffold that introduces the control necessary to select desired excitonic properties. While the ability to control photophysical processes, such as energy transport, has been established, similar control over photochemical processes, such as interchromophore charge transfer, has not been demonstrated in DNA. In particular, charge transfer requires the presence of close-range interchromophoric interactions, which have a particularly steep distance dependence, but are required for eventual energy conversion. Here, we report a DNA-chromophore platform in which long-range excitonic couplings and short-range charge-transfer couplings can be tailored. Using combinatorial screening, we discovered chromophore geometries that enhance or suppress photochemistry. We combined spectroscopic and computational results to establish the presence of symmetry-breaking charge transfer in DNA-scaffolded squaraines, which had not been previously achieved in these chromophores. Our results demonstrate that the geometric control introduced through the DNA can access otherwise inaccessible processes and program the evolution of excitonic states of molecular chromophores, opening up opportunities for designer photoactive materials for light harvesting and computation.

Identification of Nonradiative Decay Pathways in Cy3.

Photoexcited fluorescent markers are extensively used in spectroscopy, imaging, and analysis of biological systems. The performance of fluorescent markers depends on high levels of emission, which are limited by competing nonradiative decay pathways. Small-molecule fluorescent dyes have been increasingly used as markers due to their high and stable emission. Despite their prevalence, the nonradiative decay pathways of these dyes have not been determined. Here, we investigate these pathways for a widely used indocarbocyanine dye, Cy3, using transient grating spectroscopy. We identify a nonradiative decay pathway via a previously unknown dark state formed within ∼1 ps of photoexcitation. Our experiments, in combination with electronic structure calculations, suggest that the generation of the dark state is mediated by picosecond vibrational mode coupling, likely via a conical intersection. We further identify the vibrational modes, and thus structural elements, responsible for the formation and dynamics of the dark state, providing insight into suppressing nonradiative decay pathways in fluorescent markers such as Cy3.

Effect of nanotube coupling on exciton transport in polymer-free monochiral semiconducting carbon nanotube networks.

Semiconducting single-walled carbon nanotubes (s-SWCNTs) are attractive light-harvesting components for solar photoconversion schemes and architectures, and selective polymer extraction has emerged as a powerful route to obtain highly pure s-SWCNT samples for electronic applications. Here we demonstrate a novel method for producing electronically coupled thin films of near-monochiral s-SWCNTs without wrapping polymer. Detailed steady-state and transient optical studies on such samples provide new insights into the role of the wrapping polymer on controlling intra-bundle nanotube-nanotube interactions and exciton energy transfer within and between bundles. Complete removal of polymer from the networks results in rapid exciton trapping within nanotube bundles, limiting long-range exciton transport. The results suggest that intertube electronic coupling and associated exciton delocalization across multiple tubes can limit diffusive exciton transport. The complex relationship observed here between exciton delocalization, trapping, and long-range transport, helps to inform the design, preparation, and implementation of carbon nanotube networks as active elements for optical and electronic applications.

Femtosecond stimulated Raman evidence for charge-transfer character in pentacene singlet fission.

Singlet fission is a spin-allowed process in which an excited singlet state evolves into two triplet states. We use femtosecond stimulated Raman spectroscopy, an ultrafast vibrational technique, to follow the molecular structural evolution during singlet fission in order to determine the mechanism of this process. In crystalline pentacene, we observe the formation of an intermediate characterized by pairs of excited state peaks that are red- and blue-shifted relative to the ground state features. We hypothesize that these features arise from the formation of cationic and anionic species due to partial transfer of electron density from one pentacene molecule to a neighboring molecule. These observations provide experimental evidence for the role of states with significant charge-transfer character which facilitate the singlet fission process in pentacene. Our work both provides new insight into the singlet fission mechanism in pentacene and demonstrates the utility of structurally-sensitive time-resolved spectroscopic techniques in monitoring ultrafast processes.