Photophysics of J-Aggregate-Mediated Energy Transfer on DNA - The

Letter Cite This: J. Phys. Chem. Lett. 2017, 8, 5827-5833

pubs.acs.org/JPCL

Photophysics of J‑Aggregate-Mediated Energy Transfer on DNA James L. Banal,†,‡ Toru Kondo,†,§ Rémi Veneziano,‡ Mark Bathe,†,‡ and Gabriela S. Schlau-Cohen*,†,§ †

Energy Frontier Research Center for Excitonics, ‡Department of Biological Engineering, and §Department of Chemistry, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139, United States S Supporting Information *

ABSTRACT: Achieving nanoscale spatial and electronic control over the formation of dye aggregates is a major synthetic challenge due to their typically inhomogeneous self-assembly, which limits control over their higher-order organization. To address these challenges, synthetic DNA-templated pseudoisocyanine (PIC) J-aggregates were recently introduced. However, the dependence of the photophysics of the superradiant exciton on the underlying DNA template length and the impact of static disorder on energy transfer through these PIC J-aggregates remain unknown. We examine the delocalization length progression of superradiant PIC excitons by varying the length of poly-A DNA tracts that template PIC Jaggregates. We then investigate the energy-transfer efficiency from PIC J-aggregates with DNA duplex template length, which we found to be limited by static disorder. Utilizing the self-assembled and selective formation of superradiant excitons on DNA provides a platform to determine the function of delocalized excitons in the context of nanoscale energy transport.

P

to those found in photosynthetic systems, can lead to enhanced energy transfer27−29 through the interplay of both coherent and incoherent transport mechanisms.1,4 Coherently-coupled supramolecular aggregates can be readily formed in solution by control over the solvent.30 Close van der Waals interaction of the dyes in the supramolecular aggregate promotes electronic coupling of the component dyes, leading to the formation of delocalized molecular excitons. According to Kasha’s model of molecular excitons,27,31 the spatial arrangement and relative transition dipole orientations of the chromophore assemblies leads to the formation of delocalized exciton states that can be identified as either a J-aggregate, if the transition dipoles are arranged head-to-tail, or an H-aggregate, if the transition dipoles are arranged in parallel.27 The formation of J-aggregates is commonly characterized by a bathochromic shift in the absorbance spectrum. This shift is caused by the formation of a lower energy exciton state that has an enhanced oscillator strength compared with the oscillator strength of the monomer due to the linear superposition of the monomeric transition dipole moments. As a result, the radiative rates of J-aggregates are markedly enhanced relative to the monomera phenomenon termed as superradiance.32−34 Conversely, the formation of H-aggregates results in a hypsochromic shift of the absorbance spectrum relative to the lowest transition energy of the monomer absorbance spectrum and leads to suppressed radiative rates relative to the monomer. The collective radiative transition of the dyes in the J-aggregate resulting in superradiance can, in principle, also lead to coherent energy transfer, which can enhance energy-transfer rates.26 J-aggregates may be formed by spontaneous supra-

hotosynthetic light-harvesting systems consist of clustered chromophores scaffolded by protein assemblies. Absorbed energy transfers within and between these clusters over distances of 20−200 nm with near-unity quantum efficiency.1−3 The close spacing within these clusters gives rise to electronic states (excitons) that delocalize over several chromophores,1,4 resulting in the formation of an energy landscape amenable for energy transfer. Mimicking the efficient energy transfer found in photosynthetic systems requires the assembly of chromophores on the nanoscale level to have the ability to control the extent of exciton delocalization and the exciton−exciton interactions via their spatial positioning and organization. Approaches to create synthetic mimics of natural lightharvesting systems have used scaffolds that include DNA,5−13 metal−organic frameworks,14,15 synthetic proteins,16−18 and viruses.19−21 In particular, DNA has provided a programmable scaffold through which dyes can be covalently or noncovalently attached. DNA-scaffolded energy-transfer cascade systems using fluorescent cyanine intercalators, such as YO5,6,22 or bis-intercalators, such as BOBO,23 as energy relays or mediators have been demonstrated to mediate long-range energy transfer through Förster energy migration.24 Whereas the variety of scaffolds used have enabled varying degrees of control over spatial positioning, dipole orientation, and organization, the electronic coupling among the chromophores found in all of these synthetic mimics is categorized within the weak coupling or incoherent regime in which exciton delocalization is absent, in contrast with natural light-harvesting systems. Energy transport within these systems can then be described by Förster resonance energy transfer (FRET) theory.25 The formation of molecular excitons is thought to assist in realizing light-harvesting antennae that operate beyond the classical Förster regime.1,2,26 It has been predicted that energy transfer mediated by coherently coupled molecular aggregates, similar © XXXX American Chemical Society

Received: July 23, 2017 Accepted: September 20, 2017

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The Journal of Physical Chemistry Letters molecular assembly of dyes, creating either tubular or fiber-like aggregates, or alternatively through the templated assembly of the dyes.30,35−38 However, the sizes of J-aggregates prepared through these methods vary due to the inhomogeneous assembly of the chromophores and the conditions used to prepare the aggregates. This lack of control limits the ability to design artificial light-harvesting systems that require precise control over the size and position of the aggregate to direct energy transport on the nanoscale. The ability to control the spontaneous assembly of Jaggregates as well as their positioning, orientation, and higherorder spatial organization enables the creation of synthetic excitonic circuits. This control over the nanoscale positioning of discrete J-aggregates of programmed length and orientation has recently been demonstrated by templating PIC J-aggregates on poly-A tracts of B-form DNA.13 These DNA-based energy cascade circuits may, in principle, leverage molecular excitons for energy transport in numerous applications, including energy conversion.13 The extent of delocalization of the superradiant exciton and its role in enhancing energy transfer with DNA template length, however, remain unknown. Here we investigate these properties in the building block of the circuits, PIC J-aggregates on poly(dA)·poly(dT) duplexes. These duplexes serve as wirelike scaffolds5 on which PIC J-aggregates facilitate energy transfer (Figure 1). The sequence-dependent

building block in constructing light-harvesting devices through which control over the molecular and electronic structure can be used to optimize the balance of coherent and incoherent energy transfer. The addition of 5 μM DNA duplexes that contain contiguous poly(dA)·poly(dT)-tracts, termed “J-bits”,13 to a solution of 90 μM PIC in saline Tris-HCl buffer (5 mM Tris, 10 mM NaCl, pH 7.0) leads to the spontaneous formation of PIC J-aggregates templated by the DNA duplex (Figure 2). As previously

Figure 2. (a) Sequence diagram and nomenclature of DNA duplexes used in this paper. Normalized absorbance (solid line) and fluorescence of PIC (dotted line) with (b) J-bit and (c) ATA duplexes. [PIC] = 90 μM, [DNA] = 5 μM. Fluorescence spectra were measured at 490 nm excitation.

observed by Boulais et al.,13 increasing the length of the J-bit while maintaining the concentration of the duplex in the PIC solution constant results to a systematic increase in the intensity of the J-aggregate band at 550 nm in the PIC linear absorbance spectrum (Figure 2b, solid lines). For the shortest, 8-mer J-bit, the J-aggregate peak first appears as a shoulder that subsequently increases in relative intensity and transitions to a clearly distinguishable peak for the longer, 16-mer and 24-mer J-bit duplexes. Critically, DNA duplexes consisting of alternating A and T dinucleotides, abbreviated ATA, result in the unambiguous disruption of this J-aggregate signature, consistent with previous observations.13 The linear absorbance, circular dichroism (CD), and fluorescence spectra of PIC with J-bit and ATA duplexes are consistent with the observations by Boulais and co-workers13 that PIC J-aggregate formation is dependent on local DNA sequence. In particular, the linear absorbance spectra of PIC with ATA have no J-aggregate absorbance peak at 550 nm (Figure 2c, solid lines). An induced positive Cotton effect, that is, the optical rotation signal initially peaks then reaches a trough as wavelength decreases, was found to be prominent in the circular dichroism spectra of PIC with Jbit duplexes and absent in the ATA duplexes (Supplementary Figure S1). The fluorescence spectra of DNA-templated PIC J-

Figure 1. Schematic representation of PIC binding to DNA duplexes of varying tract lengths. DNA duplexes containing contiguous A-tracts template the formation of J-aggregates along the DNA minor groove. Orange DNA regions represent A-tracts, whereas white regions represent random DNA sequences.

assembly of PIC J-aggregates, similar to other cyanine dyes,39−42 allows for comparison between the radiative rates and transfer efficiencies of PIC J-aggregates and PIC monomers. Our results reveal that the superradiant exciton delocalization length and thus the energy-transfer efficiencies through the PIC J-aggregates are dependent on the length of DNA duplex and that the delocalized excited states within the Jaggregate can enhance the energy-transfer efficiency. Our results further indicate that static disorder limits the length of the DNA duplex template over which the enhancement is observed. Thus these constructs have the potential to serve as a 5828

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The Journal of Physical Chemistry Letters aggregates have a distinct sharp J-aggregate fluorescence peak at 555 nm and a broad shoulder that peaks at 600 nm (Figure 2b, dotted lines). The relative intensities of the J-aggregate fluorescence peak at 555 nm to the broad shoulder at 600 nm increase with J-bit tract length. The broad shoulder found in the emission spectra of J-aggregates has been hypothesized to be emission from exciton traps.43−45 PIC with ATA duplexes, in contrast, show a featureless broad spectra (Figure 2c, dotted lines) consistent with emission spectra observed from monomeric PIC in solution44,45 (Supplementary Figure S2). Further, we compare fluorescence excitation spectra. The excitation spectra of PIC with J-bit duplexes clearly show that the emission preferentially originates from J-aggregates, whereas excitation spectra of PIC with ATA duplexes closely mirror the absorption spectra of PIC monomers (Supplementary Figure S3). We attribute the differences between the excitation and absorbance spectra of PIC J-aggregates to the relative concentration of PIC monomers that remains in solution. To understand how the exciton delocalization of the Jaggregate13,45,46 changes with DNA template length in this work, the tract length dependence of the size of the delocalized exciton was further investigated. The radiative rate enhancement of PIC J-aggregates relative to PIC monomers was measured using steady-state and time-resolved fluorescence spectroscopy. PIC at 90 μM in saline Tris buffer in the absence of DNA duplexes has a very low quantum yield (ΦF = 0.012 ± 0.002%, mean ± s.d.). Upon the addition of 5 μM DNA duplexes in 90 μM PIC solution, an order of magnitude increase in quantum yield is observed, suggestive of PIC binding with the DNA (Figure 3a). The quantum yields of PIC J-aggregates and PIC monomers templated by DNA duplexes are enhanced as the length of the DNA tract increases, with the quantum yield of PIC J-aggregate being significantly higher (above experimental error) than the PIC monomer at 24-mer tract lengths (Figure 3a). The fluorescence lifetimes of the Jaggregates are consistently shorter across all of the J-bit tract lengths compared with PIC monomers and do not change significantly with tract length. Taking into account the quantum yields of the PIC J-aggregates and monomers, the shorter lifetime of J-aggregates compared with the monomer (Figure 3b) directly implies a radiative rate enhancement of the Jaggregates relative to the monomer that is consistent with superradiant J-aggregates.34,46 The average size of the delocalized exciton that contributes to superradiant emission (N) is estimated from the ratio of the radiative rate of the J-aggregate (kFJ) to the radiative rate of the monomer (kFM) by45

N=

kFJ kFM

=

ΦFJ τ M ΦFM τ J

Figure 3. (a) Quantum yield and (b) average fluorescence lifetime () of PIC in the presence of different duplex sequences and tract lengths. (c) Estimated size of aggregates contributing to superradiance (N). [PIC] = 90 μM, [DNA] = 5 μM. Fluorescence spectra were measured at 490 nm excitation. Error bars are standard deviations determined from independent measurements.

contrast, a red shift would be expected as a function of tract length if there were a significant increase in delocalization length (Supplementary Figure S3). As a result of these observations, the increase in quantum yield with tract length, as shown in Figure 3a, is attributed to more PIC chromophores bound on the DNA in the J-aggregate arrangement as the tract length of the duplex increases. Our data suggest that the supramolecular J-aggregates templated by increasing tract lengths are unlikely to be homogeneous or continuous, which would result in delocalization lengths increasing with tract length. Instead, our data support the formation of discrete Jaggregates with delocalization lengths of several monomers within each DNA duplex of distinct tract length, with the number of these J-aggregates per duplex increasing with tract length. Low-temperature absorbance measurements of PIC

(1)

where ΦF is the fluorescence quantum yield and τ is the fluorescence lifetime. The superscripts J and M refer to the PIC J-aggregate and PIC monomer, respectively. The exciton size increases with tract length from a value of 1.5 up to a value of 2.3, indicating that the aggregate size formed on duplexes varies by only a few constituent monomers (Figure 3c). The exciton size estimated using eq 1 is similar to estimates of coherence size based on the relative intensities of the 0−0 and 0−1 vibronic bands of the fluorescence spectra47 of PIC J-aggregates (Supplementary Figure S7). Furthermore, the excitation spectra of the PIC J-aggregates bound on DNA consistently show a Jaggregate peak at 550 nm for all J-bit duplex tract lengths. In 5829

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The Journal of Physical Chemistry Letters

PIC J-aggregates/monomers (Figure 4a). We observe a decrease in the energy-transfer efficiency of PIC to AF 647 with tract length for both the PIC J-aggregates and monomers. In this case, excitation occurs approximately evenly along the PIC binding region, including states far from the duplex end where AF 647 is conjugated. There is an observable enhancement in energy-transfer efficiency for PIC J-aggregates compared with PIC monomers for 8 and 16 tract lengths regardless of excitation wavelength (Figure 4b, Supplementary Figures S20 and S21). This energy-transfer enhancement can be ascribed to J-aggregates mediating the energy transfer to AF 647 based on the excitation spectra of PIC with DNA duplexes that are conjugated with AF 647 (Supplementary Figure S22). At 24-mer J-bit or ATA tract length, the energy-transfer efficiencies between PIC J-aggregates to AF 647 are lower compared to energy-transfer efficiencies from PIC monomers to AF 647 (Figure 4b, Supplementary Figures S20 and S21). It is remarkable that there is an observed enhancement of energy-transfer efficiency from PIC to AF 647 when Jaggregates are present for 8- and 16-mer tract lengths given that the quantum yield of PIC J-aggregates relative to PIC monomers at 8- and 16-mer tract lengths is not significantly different (Figure 3a). Quantum yield arguments based on Förster energy-transfer theory alone would therefore not be sufficient to rationalize the energy-transfer enhancement occurring in the 8-mer and 16-mer J-bit duplex constructs (Supplementary Figure S24). It can be postulated that the Jaggregates formed along the 8-mer and 16-mer J-bit duplexes facilitate efficient intermolecular energy transfer among the PIC chromophores to produce an energy-transfer rate faster than the other competing rates, such as the radiative and nonradiative rates of PIC J-aggregates. Exciton delocalization plays a complex role in intermolecular energy migration. Electronic coupling resulting in the formation of superradiant aggregates may not only facilitate energy transfer, such as in supertransfer,26 but may also redistribute oscillator strength and shift the spectral absorption bandwidth of J-aggregates relative to the monomer. The loss of energy-transfer enhancement of Jaggregate-mediated transfer relative to monomer-mediated transfer at longer tract lengths, particularly at 24-mer tract length, may be due to the inhomogeneous formation of Jaggregates with increasing tract lengths. Because there is no energy gradient along the duplex that would funnel the energy to AF 647, multiple energy migration events occur that can lead to nonradiative losses given that the quantum yield of DNAtemplated aggregates is low or that the exciton encounters a low energy trap, for example, a PIC dimer, leading to losses due to exciton trapping.43,44 Because the number of aggregates present in the J-bit duplexes increases with tract length, the probability of forming exciton traps arising from inhomogeneous binding on the DNA duplex also increases. The increase in number of exciton traps along DNA duplexes would limit the energy-transfer efficiencies to AF 647, which might explain the loss of energy-transfer efficiency to AF 647 within the 24-mer Jbit duplex template notwithstanding the high quantum yield of PIC J-aggregates bound to the 24-mer J-bit duplex. Distinguishing between these loss pathways, however, can be difficult due to the very short fluorescence lifetime of PIC in solution at room temperature.52 The results presented here reveal the progression of exciton delocalization with DNA template length and the effect of this exciton delocalization on energy-transfer efficiency. We investigated the impact of J-aggregate formation along the

with 8-mer J-bit duplex do not show any significant line narrowing (Supplementary Figure S8), even in the J-aggregate absorbance region, suggesting that static disorder is predominantly limiting the exciton delocalization length of PIC on DNA.48 Inhomogeneous binding of J-aggregates on the DNA may lead to a distribution of transition energies that can limit the size of the aggregates. Another possibility is that the helical features of the DNA itself, for example, helical pitch angle, can limit the electronic coupling of more than two chromophores if the transition dipoles of adjacent PIC chromophores cannot be maintained in the head-to-tail J-aggregate orientation. Superradiant aggregates have been postulated to enhance energy-transfer characteristics in molecular assemblies26,28,29 through supertransfer.49−51 Because of the sequence programmable assembly of PIC J-aggregates on the DNA, the energytransfer properties of the J-aggregate acting as either a donor or acceptor were studied as a function of tract length and compared with the energy-transfer properties of the PIC monomer to investigate the effect of exciton delocalization on energy transfer. The dye ATTO 390 was attached to a DNA duplex to serve as a donor to PIC J-aggregates/monomers (Figure 4a). The efficiency of energy transfer from ATTO 390

Figure 4. Energy-transfer efficiency of (a) ATTO 390 to PIC excited at 400 nm and (b) PIC to Alexa Fluor 647 excited at 545 nm. Error bars are standard deviations determined from three independent replicate measurements.

to PIC J-aggregates or PIC monomers was determined by steady-state fluorescence quenching of ATTO 390. The energytransfer efficiencies of ATTO 390 to both PIC J-aggregates and PIC monomers are comparable within experimental error and do not change with tract length (Figure 4b), which is also consistent with energy-transfer measurements determined by time-resolved fluorescence spectroscopy (Supplementary Figures S11−S13). Given that PIC J-aggregates/monomers are templated/bound near the duplex end where ATTO 390 is conjugated, most energy is expected to transfer from the ATTO 390 regardless of tract length. We then compare the efficiency of energy transfer of PIC J-aggregates/monomers to Alexa Fluor 647 (AF 647), which serves as an energy acceptor for 5830

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The Journal of Physical Chemistry Letters DNA duplex on enhancing energy transfer along DNA. We demonstrated that varying the length of the DNA poly(A-tract) does not lead to a substantial increase in the extent of exciton delocalization but instead results in increasing PIC chromophores being bound and forming J-aggregates as the tract length of the duplex increases. Our results suggest that static disorder limits the extent of exciton delocalization, with inhomogeneous J-aggregates forming along the duplex that function as trap states. We observe both tract length and PIC species dependence, that is, monomer or J-aggregate, on the efficiency of energy transfer to AF 647. Significant enhancement is observed in J-aggregate-mediated transfer to AF 647 compared with monomer-mediated transfer for 8- and 16-mer tract lengths. This energy-transfer enhancement of J-aggregates appears to be lost at 24-mer tract length, most likely because of the trap states. In contrast, comparison of the energy-transfer efficiencies of the PIC J-aggregate and the PIC monomer as energy transfer acceptor to ATTO 390 shows no significant differences in the observed efficiencies, nor does it show differences due to tract length. Detailed characterization of the photophysics and energytransfer characteristics of PIC on DNA duplexes of varying length performed here offers new insight into the extent of synthetic control feasible over the electronic properties of PIC J-aggregates templated by DNA. Moreover, we provide specific design criteria for optimizing nanoscale energy transport in excitonic circuits using DNA origami.13,53

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determined using fluorescence lifetime measurements; raw absorbance and fluorescence spectra of PIC Jaggregates and monomers in the presence or absence of AF 647; measured energy-transfer efficiencies from PIC J-aggregates/monomers to AF 647 at different excitation wavelengths; energy-transfer efficiencies from PIC Jaggregates/monomers to AF 647 at different emission wavelengths measured by TCSPC; raw concentrationdependent excitation spectra of PIC J-aggregates or PIC monomers measured by monitoring fluorescence intensity from AF 647; and calculation of spectral overlap and critical Förster distance using Förster resonance energy transfer theory. (PDF)

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

James L. Banal: 0000-0002-2364-4824 Gabriela S. Schlau-Cohen: 0000-0001-7746-2981 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported in part by the Center for Excitonics, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, and Office of Basic Energy Sciences under Award Number DE-SC0001088 (MIT), which provided funding to J.L.B., T.K., M.B., and G.S.S.-C. R.V. and M.B. also acknowledge support from the Army Research Office MURI Award No. W911NF1210420. The Biophysical Instrumentation Facility for the Study of Complex Macromolecular Systems (NSF-0070319) is gratefully acknowledged. We thank T. Sinclair and Dr. J. Caram for assistance with the low-temperature absorbance measurements.

ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpclett.7b01898. Detailed sample preparation and experimental methods for quantum yield measurements, fluorescence lifetime measurements, and energy-transfer measurements; fluorescence quantum yield benchmarking using standard reference dyes; DNA duplex sequences; absorbance and fluorescence spectra of PIC with and without DNA duplexes; excitation spectra of PIC with different lengths of DNA duplexes; transmission spectra of filters used for fluorescence lifetime measurements with time-correlated single photon counting (TCSPC); comparison of measured superradiant exciton size between 1.0 and 0.2 mm path length cuvettes; low-temperature absorbance measurements; coherence number estimates based on spectral lineshapes of PIC J-aggregates; raw steady-state absorbance and fluorescence spectra of PIC J-aggregates, PIC monomers, and ATTO 390 on DNA duplexes; fluorescence decay traces and details of fitted values of ATTO 390 in the presence or absence of PIC Jaggregates/monomers on DNA duplexes; energy-transfer efficiencies from ATTO 390 to PIC J-aggregates/ monomers with varying DNA duplex template length determined using fluorescence lifetime measurements; raw absorbance and fluorescence spectra used for determining the energy-transfer efficiency from ATTO 390 to PIC J-aggregates/monomers with different duplex lengths; fluorescence decay traces and details of fitted fluorescence decay values of PIC J-aggregates and PIC monomers in the presence or absence of AF 647 on DNA duplexes; energy-transfer efficiencies from PIC to AF 647 with varying DNA duplex template length

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DOI: 10.1021/acs.jpclett.7b01898 J. Phys. Chem. Lett. 2017, 8, 5827−5833