Tailorable Exciton Transport in Doped Peptide–Amphiphile

Tailorable Exciton Transport in Doped Peptide−Amphiphile Assemblies Lee A. Solomon,†,§ Matthew E. Sykes,†,§ Yimin A. Wu,† Richard D. Schaller,†,‡ Gary P. Wiederrecht,† and H. Christopher Fry*,† †

Center for Nanoscale Materials, Argonne National Laboratory, Lemont, Illinois 60439, United States Department of Chemistry, Northwestern University, Evanston, Illinois 60208, United States

‡

S Supporting Information *

ABSTRACT: Light-harvesting biomaterials are an attractive target in photovoltaics, photocatalysis, and artificial photosynthesis. Through peptide self-assembly, complex nanostructures can be engineered to study the role of chromophore organization during light absorption and energy transport. To this end, we demonstrate the onedimensional transport of excitons along naturally occurring, light-harvesting, Zn-protoporphyrin IX chromophores within self-assembled peptide−amphiphile nanofibers. The internal structure of the nanofibers induces packing of the porphyrins into linear chains. We find that this peptide assembly can enable long-range exciton diffusion, yet it also induces the formation of excimers between adjacent molecules, which serve as exciton traps. Electronic coupling between neighboring porphyrin molecules is confirmed by various spectroscopic methods. The exciton diffusion process is then probed through transient photoluminescence and absorption measurements and fit to a model for one-dimensional hopping. Because excimer formation impedes exciton hopping, increasing the interchromophore spacing allows for improved diffusivity, which we control through porphyrin doping levels. We show that diffusion lengths of over 60 nm are possible at low porphyrin doping, representing an order of magnitude improvement over the highest doping fractions. KEYWORDS: peptide, nanofiber, exciton, diffusion, self-assembly, doping, excimer

E

used for drug delivery, neuron migration, and mineralization reactions16−19 and more recently for photoinduced charge separation in hybrid organic−inorganic materials.20 After assembly, PAs coordinate light-absorbing molecules and act as a scaffold for chromophore arrangement.21 In this way, nanostructure and photoactivity can be independently tailored. Other biomaterials using covalently linked peptides and chromophores have also demonstrated success in solar energy conversion.10,11 However, in these systems, the scaffold is also the functional unit, making chromophore interactions difficult to modulate.22 Chromophore interactions and energy migration can be significantly modified by local conformation. In natural systems, the three-dimensional nanoscale configuration of chromophores in the light-harvesting antenna is critical to performance.4 Additionally, one should expect that chromophores in geometries such as PA nanofibers may exhibit unexpected photophysical properties. For example, it is known that low-

nvironmentally friendly materials for solar energy harvesting are actively sought by the photovoltaic and photosynthetic communities to meet society’s energy demands.1−3 Biomaterials can fulfill these needs, using natural photosystem-like processes to harness solar energy and repurpose it in new ways. In nature, plants carry out lightcapture and photoactivated electron transfer using careful arrangements of chromophores to absorb light and funnel energy to a special pair of chlorophyll molecules, which form an excimer upon photoexcitation.4,5 This excimer is used to activate the pathways to the later catalytic steps of water oxidation and carbon fixation. Many synthetic attempts have aimed to reproduce this phenomenon through the use of metal−organic frameworks,6−8 organic polymers,9 and supramolecular assemblies, utilizing metal-bound and freebase porphyrins.10−15 Whereas energy harvesting in rigid structures such as metal−organic frameworks has been well-characterized, the interplay between chromophore conformation and energy migration remains poorly understood in biomaterials. Peptide−amphiphiles (PAs) are a functionally diverse class of molecules that self-assemble into fibrous nano- to microscale biomaterial structures. Since their discovery, they have been © 2017 American Chemical Society

Received: June 1, 2017 Accepted: August 13, 2017 Published: August 17, 2017 9112

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the lysine side chains are neutralized, the PA assembles into a fibrous network (Figures 1C−H and S1). Samples were prepared by first dissolving the PA in aqueous 50 mM NH4OH and heating at 90 °C to yield nanofibers with average diameters of ∼8 nm.21,24 Then ZnP (Figure 1B) was added and the sample reheated (again at 90 °C) to promote porphyrin binding. ZnP was chosen for this study owing to its previous photophysical characterization in the literature and relative stability compared to that of other metal-centered porphyrins. Freebase porphyrins could not be used as binding requires a metal−His coordination bond. To control the porphyrin doping, we used PA at 6, 10, 20, 60, and 120 times the concentration of ZnP, which was fixed across all samples. Previous work has shown that maximal ZnP loading occurs at a ratio of 1:6 ZnP:PA (Figure S2), hence we did not exceed this ratio.21 All samples were analyzed with UV/vis spectroscopy, circular dichroism (CD) spectroscopy, and electron microscopy to ensure the porphyrin was bound and the structure was intact (Figure 2 and Figures S1 and S3). [Samples without porphyrin

dimensional systems can exhibit enhanced exciton transport distances,7,23 potentially improving their light-harvesting capabilities. Thus, PAs offer a platform to study the relationship between conformation and energy transport. Here, we investigate a PA system capable of binding Znprotoporphyrin IX (ZnP) through histidine (His) coordination, avoiding the need for covalent bonding to the peptide scaffold. In previous work, a ZnP:PA assembly was noted to exhibit exciton−exciton annihilation and a deactivation pathway of the excited state through a multiexponential process; however, the analysis was incomplete.21 Here, through rigorous photophysical characterization employing both time-resolved photoluminescence (trPL) and fluence-dependent transient absorption (TA) spectroscopies, we identify and describe the excitedstate manifold in detail and show that exciton transport is controlled by the ZnP doping level of the nanofiber assembly. We demonstrate that exciton diffusion in the doped nanofibers is mediated by excimer formation between proximal ZnP chromophores and that excimers act as efficient traps within this system. By changing ZnP doping quantities, we highlight the ability to bias energy flow toward either long-range exciton transport or rapid excimer formation. This level of control over the photophysical properties yields a tailorable material for light-harvesting or photocatalysis where one could modulate the performance via doping levels.

RESULTS AND DISCUSSION The PA employed in this study is depicted in Figure 1A. It is an 8 amino acid peptide (sequence: AHL3K3−CO2H) with palmitic acid (c16) conjugated to the amine terminus. When

Figure 2. Packing of ZnP into PA fibers confers changes to the chromophore spectra. (A) Normalized UV/vis absorption spectra and (B) zoom-in on the Soret band region showing a peak splitting at high ZnP loading. (C) Fluorescence spectra normalized to the 0 → 0 peak at 590 nm along with the excimer contribution to the 1:6 sample emission. Samples were excited at 427 nm. (D) Circular dichroism spectra of the ZnP Soret band region. All corresponding spectra for 1:10 and 1:60 samples are plotted separately in Figure S3 for clarity.

do not absorb visible light and are therefore not shown.] At ZnP doping levels (1:6 and 1:10 ZnP:PA) where the porphyrins are packed close together, we observe a splitting of the Soret band into two peaks at 420 and 430 nm (Figures 2A,B and S3A,B) in the UV/vis spectra25 and a strong Cotton effect in the CD spectra (Figures 2D and S3D). In contrast, nanofibers with lower ZnP doping levels (e.g., 1:120 ZnP:PA) exhibit a single Soret band at 427 nm, similar to that of ZnP coordinated to His in solution (Soret band: 420 nm, Figure 2A,C). The split absorption feature can be attributed to a slipped cofacial arrangement of porphyrins in the PA architecture and indicates strong electronic coupling between neighboring molecules.26 The intense CD spectra at high doping (1:6, 1:10, and 1:20) can be attributed to a large-scale ordering of interacting ZnPs throughout the chiral nanofiber environment (i.e., fixed interchromophore distance and dihedral angle along a significant length of the fiber). At low ZnP doping (1:60 and 1:120), the loss of Soret splitting and reduced CD signal can thus be explained as an increased average spacing

Figure 1. Depiction of the peptide (A) and the zinc porphyrin molecules (B, shown as both sticks and spheres) that comprise the doped nanofibers. The schematics illustrate the peptide assembly in an idealized β-sheet conformation for high doping ratios of ZnP:PA (C,E,G) and low doping ratios (D,F,H). C and D highlight the relative interchromophore packing with the high-doped system (C) yielding a proposed slipped-cofacial porphyrin arrangement. E and F illustrate the variation in porphyrin spacing. G and H highlight the fiber cross sections. 9113

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Figure 3. Time-resolved photoluminescence of the ZnP-doped PA fibers. (a) Two-dimensional map of the 1:6 ZnP:PA nanofiber photoluminescence. (b) Decay of the monomer emission as a function of doping, integrated over 560−610 nm wavelengths. (c) Decay of the excimer emission, integrated over 700−740 nm wavelengths. Red curves in b and c are fits to the data. (d) Fit of 1:6 ZnP:PA photoluminescence map through targeted analysis. (e) Species associated spectra (SAS) of the monomeric (M1) and excimeric (E1) species used for fitting and population of each species over time. (f) Jablonski diagram of exciton relaxation within the ZnP:PA system. A ZnP monomer is excited to M2 followed by fast vibrational relaxation (kVR) to the M1 state. M1 then undergoes either charge transfer to an excimer (ka) or decay to the ground state (kM). Any excimers formed are trapped and subsequently decay to the ground state (kE).

between neighboring ZnP molecules in the nanofiber, reducing the overall number of interacting porphyrins. Figure 2C shows the change in the steady-state fluorescence spectra with increased ZnP doping of the PA nanofibers. Hisbound ZnP monomers in solution exhibit two dominant vibronic peaks with emissions near 590 and 650 nm, corresponding to the 0 → 0 and 0 → 1 transitions, respectively.27,28 For ZnP-doped PA assemblies, we observe an apparent increase in the relative intensity of the 0 → 1 transition that is a direct result of an overlapping peak near 675 nm that becomes more prominent with increased doping and is distinct from the spectrum of monomeric ZnP (Figure S4). The broad and structureless emission of the 675 nm peak is characteristic of excimer states, thus we ascribe this peak to excimers formed between coupled ZnPs in the nanofiber assembly.9,28−30 Due to coordination bonding between Zn and histidine within the β-sheets (Figure 1), the ZnP molecules are organized into edge-on or slip-stacked chains necessary for excimeric interactions. To characterize the excited-state dynamics, time-resolved photoluminescence spectroscopy was employed. Samples were excited at 420 nm with a femtosecond laser, and their emission was monitored up to a 10 ns delay time. Figure 3A shows the trPL data for the 1:6 ZnP:PA doping. We observe an apparent red shift of the 0 → 1 monomer peak at ∼650 nm over time and a delayed growth of the trPL signal at longer wavelengths, whereas the position of the 0 → 0 monomer peak at ∼590 nm remains constant. Additionally, the decay of the 0 → 0 peak exhibits nonexponential behavior at early times during which the excimer signal at longer wavelengths (>700 nm) increases in intensity (Figure 3B,C). The delayed onset of the excimer peak is indicative of energy transfer to a separate emissive species from the prompt monomer fluorescence and further bolsters its assignment.29,31

Figure 3D,E shows the results from targeted analysis based on a one-dimensional (1D) diffusion-limited model of excimer formation (Supporting Information) in which we identify the population kinetics and species associated spectra (SAS) for both monomer (M1) and excimer (E1) states. The SAS are consistent across all measurements and doping concentrations and qualitatively match the steady-state spectra (Figure 2C). Additionally, Figure 3B,C shows fitted decays of M1 and E1 from targeted analysis as a function of ZnP doping. The nonexponential behavior observed at early times arises from the 1D diffusion-limited transfer of monomer excitons to excimer states.32,33 With increased ZnP doping, a larger fraction of porphyrin molecules are electronically coupled, and fewer exciton hops are required to reach an excimer site. This results in an increase in the net excimer formation rate. The intrinsic monomer and excimer decay rates, in contrast, remain relatively constant with ZnP doping (Figure S5). Thus, the overall contribution from excimer emission increases with doping, consistent with steady-state fluorescence (Figure 2B). From these data, we develop a simple Jablonski diagram for the ZnP excited states (Figure 3F). Upon excitation from the ground state (M0) to the Soret band (M2), fast vibrational relaxation occurs to the M1 state within ∼20 ps (determined from global fitting). The monomer then decays to M0 at a rate kM or associates with a neighboring ZnP to form an excimer (ka) (Figure S5). Excimer states are ∼270 meV lower in energy than monomer excitons, as determined by their peak wavelengths, and are effectively trapped without back-transfer. The excimers subsequently decay to the ground state at a rate kE (Figure S5). Due to the low quantum yields of ZnP:PA (measured to be ∼1%), the majority of both M1 and E1 decay occurs through nonradiative channels such as intersystem crossing to triplet states. However, these do not produce signals detectable in trPL data and are not discussed here. 9114

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Figure 4. Fitting of exciton−exciton annihilation in transient absorption data. (A) Transient absorption map for the 1:6 ZnP:PA sample taken at 60 μW pump power. (B) Corresponding steady-state absorbance and photoluminescence spectra, with dashed lines indicating the monomer and excimer contributions to PL. (C) Differential absorbance spectra cut at 10 and 400 ps exhibiting bleach (B) and stimulated emission (SE) features matching steady-state. The excimer SE appears absent at early times. (D) SE of the 1:6 ZnP:PA sample after background subtraction focusing on the region of the 0 → 1 and excimer peaks. Kinetic traces of SE for both the monomer (E) and excimer (F) species integrated between 635−670 and 690−740 nm, respectively. Lighter curves indicate increasing pump power spanning 60, 100, 200, 300, 400, and 500 μW, and the red curves indicate fits to the model.

To confirm the excited-state dynamics deduced from trPL measurements, ultrafast TA spectroscopy was also performed on the ZnP:PA nanofibers. Samples were pumped at 420 nm with a femtosecond laser, and their differential absorption was monitored with a white light continuum probe as a function of pump−probe delay time. Figure 4A shows a representative TA map of the 1:6 ZnP:PA sample. The TA data exhibit multiple bleach and stimulated emission (SE) features well-matched to the steady-state spectra (Figure 4B,C), overlapping a broad excited-state absorption background. The bleach features correspond to a reduction in absorption strength at the visible wavelength transitions, whereas the SE arises from probeinduced emission from the 0 → 0, 0 → 1, and excimer peaks (shown as dashed lines in Figure 4B). To selectively probe the M1 and E1 dynamics, we performed a background subtraction of the excited-state absorption (Figure S6). This procedure results in the background-free SE peaks in the 620−720 nm region (Figure 4D), corresponding to the 0 → 1 monomer and excimer emission peaks. As in the trPL data, we observe a delay of ∼400 ps in the onset of excimer emission, seen in the growth of the >680 nm emission shoulder, while prompt emission from the 0 → 1 monomer transition is observed (Figure 4C,D). Fluencedependent measurements were taken on each sample to measure the exciton−exciton annihilation dynamics, which is directly related to exciton diffusivity (Supporting Information). Figure 4E,F shows the kinetics for the 0 → 1 monomer SE and the excimer SE as a function of increasing pump fluence, and their corresponding rates are summarized in Figure S5. As can be seen, bimolecular exciton−exciton annihilation increases the

nonexponential behavior of the response at early times. Data were fitted using the same targeted analysis model as in trPL, including annihilation between monomer excitons, and we observe an excellent fit to the data (red curves in Figure 4E,F). We also note that, due to the ∼10 fs time resolution of the TA system, contributions from hot M1 states had to be included in the monomer SE, with vibrational relaxation times of ∼20 ps taken directly from global fitting. From the diffusion-limited excimer association rate ka and the exciton−exciton annihilation rate, we derive the 1D exciton diffusion length (LD) for the M1 state (Figure 5). We obtain similar values between both trPL and TA measurements, with systematic variations consistent with the literature on LD measurement methods.34 In the doping range measured, a lower density (larger separation distance) of ZnP molecules counterintuitively produces a longer LD. We observe an order of magnitude increase in LD as the ZnP doping fraction is reduced, reaching over 60 nm at a 1:120 ZnP:PA ratio. In contrast, higher ZnP doping increases the net rate of excimer formation which outcompetes the M1 diffusion process. The increase in LD with separation distance can be understood as follows. In the absence of excimer traps, Förster theory predicts that LD should decrease with distance as d−2. However, in the trap-limited regime, LD should scale with the distance between traps.35 For self-trapping processes such as excimer formation in the ZnP:PA system, the trap density and separation distance are both a function of the ZnP concentration.28,29,31 The observed increase in LD with ZnP separation distance firmly places our samples within the traplimited regime. At separation distances beyond the ZnP Förster 9115

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is an exceptional distance for incoherent exciton hopping and approaches values achieved in rigid metal−organic frameworks.8 For comparison, solid-state organic semiconductors rarely achieve LD values over ∼15 nm due to nonradiative losses.40 We attribute the above performance to the lowdimensionality of the ZnP:PA system, which forces excitons to hop in 1D, and the precise control of chromophore interactions on the nanoscale. In conclusion, this study highlights new ways to study photophysics, as well as forges a path to new aqueous bionanotechnologies based on PA materials.

METHODS Chemicals and Reagents. All chemicals and reagents used in this work were purchased from Sigma-Aldrich unless otherwise noted. Peptide Synthesis, Purification, and Characterization. The synthetic procedure for c16−AHL3K3−CO2H has been reported in our previous studies.9 The synthesis of c16−AHL3K3−CO2H, cleavage from the resin, and RP-HPLC purification followed the same strategy as the previously reported peptide, purity >98% (Figure S7A). Matrixassisted laser desorption ionization time-of-flight (MALDI-TOF) mass spectrometry (Bruker UltrafleXtreme) was used to identify the peptide; c16−AHL3K3−CO2H: calcd for C61H113N13O10 + [H+], 1188.87, found 1188.96 m/z. Sample/Stock Solution Preparation. The peptide, c16− AHL3K3−CO2H (3−4 mg), was dissolved in nanopure water (Millipore A10) to obtain a 1 wt % solution, c16−AHL3K3−CO2H (1 wt %, 8.4 mM). ZnP was dissolved in DMSO to achieve a 10 mM stock solution. Note: ZnP/DMSO stock solutions were always made to ensure that the final DMSO concentration in the sample was less than 1% (v/v). All ZnP was dissolved into DMSO to dissolve it before adding to protein samples. All ZnP stocks were kept away from light using opaque black microfuge tubes. Samples for experiments were prepared by dissolving the PA in 50 mM NH4OH and heating at 90 °C for 5 min. Samples were removed from heat, ZnP was added, and the samples reheated at 90 °C for an additional 5 min. Biophysical characterization of these assemblies can be found here.21 Mass Spectrometry. The fractions collected from HPLC purification were analyzed by MALDI-TOF mass spectrometry to confirm the mass of the synthesized peptide. Samples (1 μL) were cocrystallized with 1 μL of an α-cyano-4-hydroxycinnamic acid solution (10 mg/mL in 1:1 water/acetonitrile (0.1% TFA)) on a stainless steel MALDI plate. Calculated molecular mass was compared to experimental mass to confirm the presence of the peptide. Peptide−Amphiphile Visualization. All modeling was done in pymol version 1.4.1. Quantum Yield Measurements. To determine the quantum yield (QY), a PerkinElmer Lambda 950 UV−vis NIR spectrophotometer was used to measure concentration-dependent absorption, and the corresponding fluorescence was measured with a Horiba Jovin Yvon Nanolog fluorometer using the associated fluorescence version 3.5 software. Coumarin 153 was used as a reference standard (QY of 0.38). For all samples, the peak absorbance at the Soret band was diluted to 0.1 AU. The fluorescence excitation was set at the Soret band, and the emissions between 550 and 800 nm were collected. Each sample was diluted by 25%, and the measurements were rerun. This was done two more times for a total of four measurements per sample. The analysis was carried out as described by Brouwer. CD and UV−Vis Spectroscopy. Circular dichroism spectroscopy (Jasco, Inc. J-815) was employed to analyze the typical Cotton bands for bound ZnP in the PA fibers. Samples were prepared by diluting the ZnP to approximately 25 μM in 1 mm cuvettes. In order to get electronic absorption data, used to monitor porphyrin binding and degradation, we used a Varian Cary 50 scan spectrophotometer. Samples were prepared as above and diluted to 25 μM unless otherwise noted. Gaussian peak fitting was then used to separate the monomer and excimer contributions to the emission spectra. All samples prepared in 50 mM NH4OH. UV/vis and fluorescence: 5 μM ZnP, commensurate protein based on sample. CD: 25 μM porphyrin,

Figure 5. Exciton diffusion length (LD) as a function of intermolecular separation distance (d) derived from transient photoluminescence (red circles) and transient absorption (blue squares) spectroscopies.

radius (∼3 nm), we expect a reduction in LD as the hopping rate progressively diminishes. Indeed, we observe a leveling off of LD between 1:60 and 1:120 ZnP:PA, thus we expect these values to be near the maximum LD of this system (Figure 5). However, due to gelation at higher PA concentrations and signal loss at lower ZnP concentrations, we were unable to further reduce the porphyrin doping.

CONCLUSIONS We have presented a system conceptually similar to natural photosynthetic complexes, where energy is absorbed by an array of chromophores and funneled into excimeric pairs. The simplicity of the PA framework provides an excellent tool to study the effects of the protein environment on artificial photosynthetic processes. The 8 amino acid sequence removes much of the complexity inherent in natural systems, highlighting the most basic engineering principles needed for functional light harvesting. With simple changes to the PA assembly, through either sequence or environmental conditions, the effects on chromophore photophysics can be easily and systematically investigated. Due to the design flexibility afforded by the PA scaffold, future studies with other chromophores (e.g., chlorophyll or other light-harvesting porphyrins) and their conformations may unlock longer range coherent processes,36,37 which have been shown to enable the high efficiencies of natural photosystems.38 The incorporation of multiple sequences of peptides or multiple chromophores within an assembled nanostructure may also enable the assignment of site-specific locations for energy harvesting and electron transfer. Additional studies are also underway to investigate the effects of the peptide backbone on chromophore interaction. Finally, related PA systems have shown the ability to self-heal,39 a property that sets PA assemblies above current technologies. Combined, these parameters could lead to a light-harvesting system that can repair when damaged. Our simple PA system can bind ZnP, producing a distribution of monomers as well as closely spaced ZnP that can form excimers, the ratio of which we can control through doping level. Thus, we are able to bias the ZnP:PA system toward either exciton transport at low concentrations of ZnP or excimer formation at high concentrations. At low concentrations, we have demonstrated LD values of over 60 nm, which 9116

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ACS Nano 2 mm cuvette. In ZnP samples, PA was substituted with a 1 M His buffer; 1:10 and 1:60 sample spectra moved to Figure S3 for clarity. Electron Microscopy. Transmission electron microscopy (TEM) was performed with a JEOL 2100F operated at accelerating voltage of 200 kV and equipped with a Gatan imaging filter system at the Center for Nanoscale Materials, Argonne National Laboratory. TEM samples were prepared by drop-casting peptide NH4OH aqueous solution onto lacey carbon grids. Samples of varying concentrations were diluted 100-fold in water and drop-cast onto a 400 mesh copper grid with a carbon support film (Ted Pella). After 1 min, the excess solution was wicked away and the sample air-dried. Streak Camera Photoluminescence. Time- and wavelengthresolved photoluminescence data were acquired using a pulsed laser and streak camera detection system. Specifically, a 35 fs pulse width, amplified Ti:sapphire laser operating at 2 kHz pumped an optical parametric amplifier to produce 420 nm pump pulses, which were directed into the sample. Photoluminescence was collected with a lens and directed to a 150 mm focal length spectrograph and single-photon sensitive streak camera. The nitrogen-purged samples were stirred in a 2 mm quartz cuvette during the course of the measurement. The pump power was controlled by a variable neutral density filter and maintained within the linear excitation regime, well below the onset of exciton−exciton annihilation. Multiple measurements at varying pump power were performed on each sample for confirmation. For each power, measurements were performed with both a short (2 ns) and long (10 ns) time window to capture both the fast dynamics of excimer formation and slow fluorescence decay of ZnP, and the data sets were subsequently merged. Transient Absorption Spectroscopy. Time-resolved TA measurements were performed with a commercial transient spectrometer (Newport Helios). Pump and probe pulses were derived from a regeneratively amplified Ti:sapphire laser (Newport Tsunami and SpitFire Pro), which produced 120 fs pulses at 5 kHz. A pump wavelength of 420 nm was used for all measurements, whereas a white light continuum probe was generated from a sapphire crystal. The incident pump power was adjusted with a variable neutral density filter and calibrated with a power meter, and its diameter was determined to be ∼300 μm at the sample. Pump fluences were varied within the nonlinear excitation regime, confirmed both by the saturation of the transient absorption signal and the presence of exciton−exciton annihilation. The nitrogen-purged samples were stirred in a 2 mm quartz cuvette during the course of the measurement. Each data set represents an average of 3−5 measurements. Prior to further analysis, data were chirp-corrected with SurfacePro software, version 4.1.0 (Ultrafast Systems, LLC). Global Analysis. Both trPL and TA data sets were globally fit to multiexponential decays using the software package Glotaran version 1.5.1. The trPL data were fit to a triexponential decay with a Gaussian instrument response function (IRF), whereas TA data were fit using six exponential decays and Gaussian IRF. The time-zero of the IRF was used to temporally align the trPL data sets during merging, whereas the IRFs for both trPL and TA measurements were employed during targeted analysis. Targeted Analysis. The wavelength-dependent kinetics of the trPL and TA data sets were subsequently fit to the photophysical model of Figure 3f after global analysis. In both cases, the monomer and excimer kinetics can be described by the following rate equations:

d[M1] = − ka(t )[M 0][M1] − kM[M1] − 0.5kMM(t )[M1]2 dt

(1)

d[E1] = ka(t )[M 0][M1] − kE[E1] dt

(2)

ka(t ) =

2πDR2 πDt

(3)

and

kMM(t ) =

2 4πDRMM 2πDt

(4)

where R and RMM are the corresponding interaction radii for excimer formation and exciton−exciton annihilation. For the trPL measurements, pump fluences were kept low enough that annihilation could be neglected along with the third term in eq 1. However, the TA measurements were performed at much higher fluences, and the annihilation term had to be included in the fitting. The bimolecular rate constants of eq 3 and eq 4 were then used to determine the LD according to the relation LD = 2DτM , where τM is the lifetime of the monomer. Further details on the targeted analysis procedure can be found in the Supporting Information.

ASSOCIATED CONTENT S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.7b03867. TEM micrographs of drop-cast nanofiber bundles, HPLC and mass spectroscopy data, UV/vis and CD spectra, ZnP titration curves, details of targeted analysis and TA background subtraction, and rate constants extracted from trPL and TA fitting (PDF)

AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected]. Author Contributions §

L.A.S. and M.E.S. contributed equally to this work.

Notes

The authors declare no competing financial interest.

ACKNOWLEDGMENTS This work was performed at the Center for Nanoscale Materials, a U.S. Department of Energy Office of Science User Facility and supported by the U.S. Department of Energy, Office of Science under Contract DE-AC02-06CH11357. The authors would like to thank David Gostzola for his help with transient absorption experiments. REFERENCES (1) Park, H.; Heldman, N.; Rebentrost, P.; Abbondanza, L.; Iagatti, A.; Alessi, A.; Patrizi, B.; Salvalaggio, M.; Bussotti, L.; Mohseni, M.; Caruso, F.; Johnsen, H. C.; Fusco, R.; Foggi, P.; Scudo, P. F.; Lloyd, S.; Belcher, A. M. Enhanced Energy Transport in Genetically Engineered Excitonic Networks. Nat. Mater. 2015, 15, 211−216. (2) Ahrens, M. J.; Sinks, L. E.; Rybtchinski, B.; Liu, W.; et al. SelfAssembly of Supramolecular Light-Harvesting Arrays From Covalent Multi-Chromophore Perylene-3, 4:9, 10-Bis (Dicarboximide) Building Blocks. J. Am. Chem. Soc. 2004, 126, 8284−8294. (3) Kim, J. H.; Nam, D. H.; Park, C. B. Nanobiocatalytic Assemblies for Artificial Photosynthesis. Curr. Opin. Biotechnol. 2014, 28, 1−9. (4) Scholes, G. D.; Fleming, G. R.; Olaya-Castro, A.; van Grondelle, R. Lessons From Nature About Solar Light Harvesting. Nat. Chem. 2011, 3, 763−774. (5) Croce, R.; van Amerongen, H. Natural Strategies for Photosynthetic Light Harvesting. Nat. Chem. Biol. 2014, 10, 492−501. (6) So, M. C.; Wiederrecht, G. P.; Mondloch, J. E.; Hupp, J. T.; Farha, O. K. Metal−Organic Framework Materials for Light-

Here, the brackets denote concentration, kM and kE are the intrinsic monomer and excimer decay rates, and ka and kMM are the diffusionlimited bimolecular rates of excimer association and exciton−exciton annihilation, respectively. Both bimolecular rates are time-dependent due to the nature of the 1D diffusion process and are related to the exciton diffusivity (D) through 9117

DOI: 10.1021/acsnano.7b03867 ACS Nano 2017, 11, 9112−9118

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DOI: 10.1021/acsnano.7b03867 ACS Nano 2017, 11, 9112−9118