Charge Separation and Recombination Pathways in Diblock DNA

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B: Biophysics; Physical Chemistry of Biological Systems and Biomolecules

Charge Separation and Recombination Pathways in Diblock DNA Hairpins Jacob H. Olshansky, Ryan M. Young, and Michael R. Wasielewski J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.8b11782 • Publication Date (Web): 18 Jan 2019 Downloaded from http://pubs.acs.org on January 22, 2019

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The Journal of Physical Chemistry

Charge Separation and Recombination Pathways in Diblock DNA Hairpins Jacob H. Olshansky, Ryan M. Young, and Michael R. Wasielewski* Department of Chemistry and Institute for Sustainability and Energy at Northwestern Northwestern University, Evanston, IL 60208-3113, U.S.A. *[email protected]

1 ACS Paragon Plus Environment

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ABSTRACT: Achieving high-yielding photoinduced charge separation through the π-stacked bases of DNA is a critical requirement for realizing numerous DNA-based technologies. In the current work, we combine two strategies for achieving high-yield charge separation. First, a chromophore with a high driving force for charge injection, naphthalenediimide (NDI), is used since it generates hot carriers that enhance charge transfer rates. Second, a diblock DNA sequence is used with two or three adenines followed by a series of guanines to implement an energy landscape that accelerates charge separation while retarding charge recombination. The photoinduced dynamics of these NDI diblock oligomers with and without a terminal hole acceptor are probed by femtosecond transient absorption spectroscopy. The measured rate constants for various charge separation and recombination processes are interpreted within the context of a full kinetic model of these systems. We find that the A2 and A3 oligomers achieve similar charge separation yields (as high as 20-25%) for a given length, yet the critical recombination process that determines these yields occurs at different distances from the NDI chromophore and on different time scales. This type of analysis could be used to predict charge separation efficiencies in candidate DNA structures.


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INTRODUCTION The observation that the DNA double helix can conduct charge through π-stacked bases has sparked intense research efforts over the past two decades.1-3 These efforts have predominantly been aimed towards either understanding the role of charge conduction in biological processes4-7 or towards harnessing this conductivity for molecular electronics applications.8-10 In both cases, the mobile charges can be generated by photoexcitation and subsequent charge separation. Such photoinduced processes have been implicated in DNA photo-damage mechanisms,7 and are potentially useful in designing DNA-based optoelectronic devices.10 Therefore, building a detailed understanding of photoexcited charge separation in DNA is of broad interest. Specifically, developing design rules for achieving high-yield charge separation in DNA is beneficial to any light-based molecular electronics application that utilizes DNA. There are a handful of reports from our collaboration with the Lewis group on DNA hairpins that give relatively high-yield charge separation efficiencies with long-lived charge separated states.11-13 In these structures, a chromophore typically serves as the hairpin linker. Photoexcitation of this chromophore results in hole transfer to a purine that can in turn support hole transfer to adjacent purines down the DNA sequence. The synthetic DNA hairpins are also often functionalized with molecular end caps that can serve as terminal hole acceptors. The efficiency of the charge separation in these synthetic structures is determined primarily by two features: the identity of the hairpin linker chromophore and the specific DNA sequence. To achieve high-yield charge separation, the chromophore should be chosen with energetics that support fast charge injection and slow charge recombination. Similarly, the DNA sequence should be designed with the same goals in mind.



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The importance of the chromophore is illustrated by comparing the charge separation yields across six A-T pairs with different chromophores. Diphenylacetylene, stilbenedicarboxamide (Sa), and naphthalenediimide (NDI) hairpin linkers give charge separation yields of 28%,11 9%,13 and 1.0 - 10%,12, 14 respectively, while a perylenediimide (PDI) base pair surrogate gives a yield of < 5%.15 Although the precise value of these reported yields may vary according to the spectroscopic means by which they are obtained, the range of yields indicates the importance of chromophore identity. As for the impact of the DNA sequence on yield, it has been shown that diblock DNA sequences with consecutive A and G blocks can promote enhanced charge separation while preventing charge recombination, since holes localized on guanine must transfer energetically uphill to get back to the A-block. Yields in DNA hairpins with Sa improved from 9% to 30-32% when replacing six A-T base pairs with a diblock sequence composed of two or three adenines followed by guanines (A6 vs. A2G4 or A3G3).13 Significant theoretical work has been performed to better understand the mechanism of charge transport in DNA systems,1, 16-19 including the photoexcited DNA-chromophore systems described above.12, 20-26 Much of this work has been performed on A-tract (or poly(A)) sequences, leading to a consensus that charge transport is dominated by the highly distance-dependent process of tunneling (superexchange) for short A-tracts and

a process with a more gradual distance

dependence for longer A-tracts, traditionally assigned to incoherent hopping.16,

21, 27

This

observation is further confirmed by experimental work.28-29 The transition between the two regimes occurs at about four base pairs, which further justifies the use of the diblock sequences described above, with A2 or A3, for enhancing charge separation. This is because charge transport through longer A-tracts would rely on incoherent charge hopping that could lead to enhanced recombination. It should be noted that recent work has provided a richer understanding of DNA


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charge transport, beyond superexchange vs. hopping. Structural fluctuations in DNA that give rise to a dynamic energy landscape have been proposed to gate resonant charge transfer in the flickering resonance mechanism, important for short distances.20, 30 At longer distances, charge delocalization over multiple degenerate base pairs has been proposed to mediate the classical incoherent hopping mechanism.21 Despite this extensive work, theoretical kinetic treatments of charge transport in diblock DNA are lacking. There are a few examples of theoretical treatments of short DNA hairpins with an Atract and one guanine that show charge separation efficiency increases with the addition of guanine.21,

24

Nevertheless, fundamental questions remain about charge transfer in diblock

sequences: What is the optimal length of the A-tract? Why are yields for the A2Gm and A3Gm oligomers indistinguishable for the previously reported diblock DNA study with Sa?13 In the current study we hope to address these questions while also exploring a DNA photoexcited charge separation system that combines the benefits of a diblock sequence with a strongly oxidizing chromophore in NDI. The large driving force for initial charge injection presented by NDI has been posited to result in enhanced hole injection and propagation owing to hot hole states.12 However, NDI hairpins have not previously been reported with the diblock sequences that tend to enhance charge separation efficiencies. Therefore, we aim to explore how charge separation efficiencies in NDI-based DNA hairpins are affected by base pair sequence, specifically the length of the A-tract in diblock oligomers. We have investigated diblock NDI hairpins with and without a terminal hole acceptor, stilbene-4,4-diether (Sd), to better isolate the charge transfer processes associated with the DNA base pairs and the Sd respectively. Furthermore, we dissect the kinetics of the various charge transfer and recombination processes that dictate charge separation efficiency and compare the



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results with a kinetic model based on Marcus theory in hopes of developing a generalizable model for engineering high-yield charge separation in DNA.

EXPERIMENTAL DNA

Synthesis,

Purification,

and

Characterization.

The

syntheses

of

bis(2-

hydroxyethyl)stilbene-4,4’-diether (Sd)31 and N,N’-[bis-(3-hydroxypropyl)]-naphthalene-1,4:5,8bis(dicarboximide) (NDI)32 have been described previously, and served as the diol precursors for the mono substitutions of dimethoxytrityl followed by conversion to their respective cyanoethylN,N-diisopropyl phosphoramidite derivatives.33 These derivatives were used with conventional cyanoethyl phosphoramidite reagents in an oligonucleotide synthesizer (Expedite, 8900) to produce the desired DNA hairpins. Hairpins were purified by reverse phase gradient HPLC and characterized by MALDI-TOF mass spectrometry, UV-Vis spectroscopy, and circular dichroism spectroscopy. Further details can be found in the Supporting Information (SI). Optical Spectroscopy. All optical measurements were performed at room temperature in aqueous solutions of 100 mM sodium chloride and 10 mM sodium phosphate buffer (pH = 7.2). Solutions were prepared to achieve an optical density of ~0.5 at λexc = 355 nm in 2 mm cuvettes. This corresponds to concentrations of the DNA hairpins of 100-150 µM. Solutions were deaerated with bubbling nitrogen in a septa-capped cuvette for ~15 min prior to transient absorption experiments. Details of the transient absorption instrumentation have been described previously,34 and are summarized in the SI.

RESULTS AND DISCUSSION


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Structures and Energetics. The DNA structures explored in this study are shown in Scheme 1. All structures are DNA hairpins with an NDI electron acceptor (hole donor) as the hairpin linker. The hairpins are composed of two complementary DNA sequences. The electronically active sequence is composed of an A-tract (m base pairs), followed by a G-tract (n base pairs), which act as electron donors (hole acceptors) with progressively less positive oxidation potentials. Therefore, photoexcitation of NDI results in exergonic hole transfer to the adjacent A-tract, which can in turn lead to exergonic hole transfer to the G-tract. Structures were synthesized with and without a terminal hole acceptor, Sd, to isolate the dynamics in just the A and G tracts. The lengths of the A and G tracts are varied to better understand the key factors in obtaining high-yield charge separation. Specifically, the A-tract length is fixed at either two or three base pairs, and the G tract lengths range from one to six base pairs. The lengths of the A-tract were chosen since they are believed to be the best compromise between efficient charge separation (i.e. the hole reaching the G-tract), and slow charge recombination from the spatially separated G-tract. This is informed by our previous work with diblock oligonucleotides composed of A and G tracts using Sa as the hole donor. In that work, conjugates with A-tracts of two or three base pairs adjacent to G-tracts were demonstrated to produce the highest charge separation yields of hole transfer to the terminal Sd hole acceptor.13



Scheme 1. DNA hairpin structures and energetics. (a) Structure of NDI and Sd. (b) Hairpin structures synthesized; m and n represent the lengths of A and G tracts respectively. (c) Relative energies of the ion pairs upon photoexcitation of NDI. The optical absorption of select hairpins is shown in Figure 1. All structures have absorption features at 385 nm and 364 nm that are associated with the absorption of NDI. The NDI-AmGn-Sd conjugates exhibit additional absorption features at 345 nm and 328 nm that are associated with Sd absorption. It is clear from the figure that the relative absorption of the NDI and Sd features is constant across all NDI-AmGn-Sd structures. This is consistent with the presence of one NDI and one Sd on each conjugate. The DNA base pairs absorb at 260 nm, so longer hairpins absorb more strongly in this region, as can be seen in Figure 1. Absorption spectra of all hairpins studied can be found in the SI. Circular dichroism spectroscopy was also performed on all structures in buffer to confirm that they fold into B-form double helices (SI). B-form DNA helices have been welldocumented as hole transfer conduits, with charges transferring between π-stacked purines.3


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Figure 1. Optical absorption of select hairpins with (blue) Sd and without (red) Sd, normalized to the absorption at 385 nm. Inset: expansion of the NDI and Sd absorption region to highlight the degree of co-excitation at 355 nm.

Photoexcitation of NDI initiates hole transfer in these systems, so the transient experiments would ideally be performed by selectively photoexciting NDI (e.g. at 380 nm). However, instrument limitations required an excitation wavelength of 355 nm. As can be seen in the Figure 1 inset, this wavelength also corresponds to a non-zero Sd absorption. Approximately 25% of 355 nm photons will be absorbed by Sd and the rest by NDI. This will play an important role in processing the transient absorption data but is shown to not affect the observed dynamics of the primary hole transfer process under investigation. The relevant energetics of the DNA hairpins are shown in Scheme 1c and have been well established by our previous work.12, 32 The Gibbs free energy change for the initial charge injection from photoexcited NDI to A is ΔGinj = -1.02 eV. Hole transfer from the A-tract to the G-tract is associated with an energy of ΔGCT = -0.45 eV, and charge transfer from G to Sd has ΔGCT = -0.51 9 ACS Paragon Plus Environment


eV. A full table of relevant free energy changes is provided in the SI. It is worth commenting on how these driving forces for charge transfer fit within the Marcus framework for understanding DNA charge transfer systems. The total reorganization energy for charge transfer in similar DNA hairpins has been found to be ~1.0-1.2 eV.32 Therefore, charge injection from NDI to A is near the barrierless region with a maximal rate, while transfer from A to G or from G to Sd operates in the Marcus normal regime, and the relevant charge recombination pathways are in the Marcus inverted regime. Dynamics of NDI-Am-Gn Structures. Photoinduced charge transfer in these structures was studied by ultrafast transient absorption spectroscopy. In this experiment, a femtosecond laser excites the NDI at 355 nm, and the resultant photophysical processes are monitored with subpicosecond time resolution using a broadband probe (380 – 650 nm). In the NDI-Am-Gn hairpins, only NDI is excited. Upon photoexcitation,

1*NDI

is converted to NDI•- via hole transfer to an adjacent adenine.

This process occurs on the timescale of the ca. 150 fs instrument response since spectroscopic features indicative of 1*NDI (595 nm) are apparent in the first 200 fs but convert to NDI•- by ~300 fs (see Figure 2a). This is consistent with what has been reported earlier for NDI-A charge transfer.32, 35 Furthermore, a full Marcus model based on a compilation of rates at varying driving forces in DNA indicate that this process would occur in ~130 fs.32 A high charge separation quantum yield is evidenced by three observations. First, the only competitive deactivation pathway for 1*NDI is intersystem crossing (ISC), which has been shown to have a 10 ps (in chloroform)36 or 14 ps (diol in methanol)35 time constant but may be as fast as 2 ps according to a mechanism involving a pre-equilibrium with high energy triplet states.37 In either case, the ~200 fs charge separation far outcompetes ISC. Second, there is no significant change in the magnitude of the


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1*NDI/NDI-•

transient spectra in the first few hundred femtoseconds, thus precluding significant

ISC, which would both deplete the signal and generate a new Tn  T1 absorption feature near 450 nm.37 Third, using the bleach of the NDI ground state as an internal quantum yield standard, and relying on the measured extinction coefficients for NDI and NDI•-,38 the measured A of NDI•after it is fully formed indicates that its quantum yield of formation is 85%.

Figure 2. Transient absorption data for NDI-AmGn hairpins following ~60 fs, 355 nm excitation (1.0 µJ/pulse). (a) Transient spectra at different times for a representative structure: NDI-A3G2. (b) Time traces of NDI•- (normalized ΔA at 488 nm) for NDI-AmGn structures with (magentared) NDI-A2Gn structures, (green-blue) NDI-A3Gn structures, and (black) kinetic fits overlain.

After this initial charge separation, the time-resolved absorption spectra are dominated by absorptions belonging to NDI•- at 487, 538, and 615 nm, and the ground-state bleach at 380 nm. It should be noted that absorption features from G•+ and an (A)n•+ polaron have previously been observed at 575 nm and 565 nm respectively. However, the polaron absorption was quite broad and weak for structures with two or three adenines, and the G•+ feature only appeared when the guanine was one or two base pairs away from the chromophore.11 Additionally, the spectra do not 11 ACS Paragon Plus Environment


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discernibly change shape over time, or between different samples. The spectra shown in Figure 2a are therefore interpreted as the decaying population of NDI•-. The absorption of the NDI•- is shown as a function of time for multiple NDI-Am-Gn hairpins in Figure 2b. The time traces at positive time delays were fit to tri-exponential decays in accordance with eq 1 (with i = 3). ∆𝐴(𝑡) =

∑

( )

𝛼𝑖 ∗ exp ― 𝑖=1

𝑡 + 𝛼0 𝜏𝑖

(1)

The results of these fits are shown in Table 1. All hairpins show a significant 2-3 ps decay feature, which is assigned to the recombination of the contact ion pair of NDI•- and the neighboring cationic adenine.32,

35

These data show a clear difference between the NDI-A2-Gn and NDI-A3-Gn

structures. Notably, the NDI-A2-Gn structures exhibit less contact ion pair recombination (α1 is smaller), but have a significant ~50 ps decay compared to the NDI-A3-Gn structures. This is likely a result of the proximity between the G-tract and NDI in the NDI-A2-Gn case that enables both faster hole transfer to the G-tract and faster charge recombination from the G-tract. In fact, all NDI-A2-Gn samples display complete charge recombination within the 8 ns experiment window. In contrast, the NDI-A3-Gn structures achieve long-lived charge separation (>8 ns) since the three adenine bases between the G-tract and NDI serve as a barrier to charge recombination. Hole transport dynamics within the G-tract are also evidenced in all structures by the fact that longer Gtracts result in longer lived charge-separated species. A more quantitative analysis of the different charge dynamics in the A2 and A3 structures was performed using a kinetic model informed by the data from the NDI-Am-Gn-Sd structures, and is discussed in a later section.


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Table 1. Time Constants () and Normalized Amplitudes () for NDI•Decay in NDI-Am-Gn Hairpins hairpin NDI-A2-G1 NDI-A2-G3 NDI-A2-G4 NDI-A3-G1 NDI-A3-G2 NDI-A3-G3 NDI-A3-G4 NDI-A3-G5

τ1 (α1) (ps)a 2.1 (65) 2.1 (63) 2.1 (63) 2.7 (81) 2.6 (80) 2.7 (79) 2.8 (79) 2.9 (79)

τ2 (α2) (ps)b 50 (26) 47 (18) 48 (17) 58 (6) 94 (6) 84 (5) 100 (5) 67 (6)

τ3 (α3)c (ns) 0.15 (9) 0.53 (19) 0.81 (18) 2.8 (12) 2.4 (11) 1.6 (9) 2.6 (9) 2.2 (7)

aFitting

errors were ~0.1 ps. bFitting errors were ~10 ps and 30-40 ps for NDI-A2Gn and NDI-A3-Gn structures respectively. c Fitting errors were quite large (due to the 8 ns time window).

Dynamics of NDI-Am-Gn-Sd Structures. Femtosecond transient absorption spectroscopy was used to probe the charge transfer dynamics in the NDI-Am-Gn-Sd structures in the same manner as was described for the NDI-Am-Gn structures. The transient data were analyzed by separating each spectrum into NDI•- and Sd•+ components that enabled orthogonal tracking of charge arrival at Sd and recombination to NDI. As discussed above, the 355 nm excitation will excite both the NDI and Sd for these structures. The normalized absorption spectra from Figure 1 indicate that Sd will absorb ~25% of the incident 355 nm photons. It is therefore unsurprising that the transient spectra for NDI-A3-G2-Sd, shown in Figure 3a, display an Sd-associated feature within the instrument response along with the NDI•features that were observed in the NDI-Am-Gn structures (Figure 2a). Specifically, the new feature at 538 nm is assigned to the presence of Sd•+ generated by electron transfer to cytosine within the instrument response. Electron transfer from Sd as a hairpin linker to adjacent cytosine or thymine bases has been observed previously to occur faster than 0.2 ps. In that work, the charge recombination times for the resultant Sd•+/C•- and Sd•+/T•- ion pairs were measured at 13 and 32 ps, respectively and were associated with a complete decay of the stilbene radical.39 More recent studies have suggested that 1*Sd to Sd•+/C•- electron transfer is a reversible process with 2.5 ps time 13 ACS Paragon Plus Environment


constants.40 In both studies, electron migration is not observed in these hairpins, consistent with the poor orbital overlap between adjacent pyrimidines.41 Therefore, Sd absorption will possibly complicate the analysis in the first tens of picoseconds, but can be accounted for and does not interfere with interpretation of the NDI-borne hole dynamics of interest at longer times. To analyze the NDI•- kinetics separately from those of Sd•+, a spectral deconvolution was performed on the transient spectra at each time point. The basis spectrum for NDI•- is an average of the NDI-Am-Gn transient spectra, which only show appreciable absorption from the anion radical. The Sd•+ basis spectrum was then derived by subtracting the NDI•- spectrum from the longtime data (>500 ps) of the 4 and 5 base pair NDI-Am-Gn-Sd hairpins, which were assumed to be associated with a one-to-one NDI•-/Sd•+ (Figure 3b, black trace). It should be noted that this longtime NDI•-/Sd•+ spectrum was indistinguishable between sequences, further supporting its assignment (See SI for transient spectra of all sequences). Similar results were also obtained using the previously reported Sd•+ basis spectrum.42 Representative results from the spectral deconvolution are shown in Figures 3c,d as relative populations of NDI•- and Sd•+ over time. Data are normalized such that the initial NDI•- population is unity. All structures also showed initial Sd•+ population resulting from co-excitation and rapid electron transfer, as discussed above. This initial population is predicted to be 0.34 according to the relative absorption ratios (~25% of photons absorbed by Sd vs. ~75% NDI), consistent with the measured average initial Sd•+ population of 0.29 ± 0.04 across all twelve NDI-Am-Gn-Sd hairpins.


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Figure 3. Transient absorption data for the NDI-AmGn-Sd hairpins following ~60 fs, 355 nm excitation (1.0 µJ/pulse). (a) Transient spectra at different times for a representative structure: NDI-A3G2-Sd. (b) Basis spectra of (red) NDI•-, (blue) Sd•+, and (black) the long-lived NDI•/Sd•+ state used to deconvolve the transient spectra into NDI•- and Sd•+ populations. (c-d) Time traces of (red) NDI•- populations, (blue) Sd•+ populations, and (black) kinetic fits for two representative structures.

Independent kinetic fits of the NDI•- and Sd•+ populations using eq 1 are shown in Figure 3c,d and parameters are given in Table 2. The NDI•- populations exhibit many of the same characteristics seen in the NDI-Am-Gn hairpins. In particular, the first two time constants and 15 ACS Paragon Plus Environment


associated amplitudes show the same behavior as in the NDI-Am-Gn structures, since they reflect the dynamics of hole propagation and recombination in the A-tract and early part of the G-tract and are therefore unaffected by Sd at the end of the hairpin. As in the NDI-Am-Gn structures, the 2-3 ps NDI•--A•+ contact ion recombination is consistently more prominent in the A3 hairpins (7679%) compared to the A2 hairpins (62-64%), while the A2 hairpins exhibit a more significant ~40 ps decay feature (13-18%). In contrast with the NDI-Am-Gn hairpins, the A2 structures display long-lived charge separation since the hole is trapped at Sd before it can recombine from the Gtract. The timescale of this hole trapping can be determined by examining the Sd•+ dynamics. The stilbene cation population was also fit to eq 1 with a negative value of α2 to reflect population growth in Sd•+ from hole migration. The values of τ1 are associated with recombination from the Sd•+/C•- and Sd•+/T•- states generated upon photoexcitation and have values of 5-6 ps and ~30 ps respectively, consistent with prior reports mentioned above.39-40 The long Sd•+/T•- recombination present in NDI-Am-Sd structures obscures the Sd•+ formation time, preventing accurate determination of τ2. The other NDI-Am-Gn-Sd hairpins show a marked trend in τ2 values, increasing with the length of the hairpin. A third exponential was required for the shortest (four base pair) hairpins to reflect recombination between NDI•- and Sd•+. The full recombination dynamics were obtained from nanosecond transient absorption and are shown in the SI. Although there is some recombination on the 1-10 ns timescale, most of the NDI•- and Sd•+ recombination occurs in 2-3 µs (four base pairs), 30-40 µs (five base pairs), and >50 µs for longer hairpins. Furthermore, there are no spectral features associated with the triplet of NDI,36 which at 2.03 eV43 is higher in energy than the 1.28 eV NDI•- / Sd•+ state. Therefore, charge recombination is expected to proceed to the


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ground state. Key metrics of the NDI-Am-Gn-Sd hairpins are summarized in Figure 4, which shows the Sd•+ formation rate constant and charge separation yields as a function of sequence length. The formation time constant, kSd+, is simply the inverse of τ2 from Table 2 (for Sd•+) and is seen to Table 2. Time constants () and normalized amplitudes () for NDI•- and Sd+• dynamics in NDI-Am-Gn-Sd hairpins hairpin NDI-A4-Sd NDI-A5-Sd NDI-A2G2-Sd NDI-A2G3-Sd NDI-A2G4-Sd NDI-A2G5-Sd NDI-A2G6-Sd NDI-A3G1-Sd NDI-A3G2-Sd NDI-A3G3-Sd NDI-A3G4-Sd NDI-A3G5-Sd NDI-A3G6-Sd

NDI•- dynamicsa τ1 (α1) (ps) τ2 (α2) (ps) 3.0 (80) 33 (6) 2.9 (84) 18 (10) 2.5 (63) 37 (13) 2.4 (64) 51 (18) 2.4 (62) 38 (18) 2.6 (64) 44 (17) 2.4 (65) 51 (18) 2.7 (79) 67 (2) 2.8 (79) 43 (5) 2.9 (79) 57 (5) 2.9 (78) 52 (6) 3.2 (76) 69 (6) 3.2 (75) 62 (7)

τ3 (α3) (ns) 5.6 (6) 0.10 (1) 1.3 (4) 0.81 (4) 0.39 (12) 0.69 (12) 0.96 (12) 15.2 (18) -2.2 (5) 1.6 (5) 1.8 (7) 2.2 (7)

Sd•+ dynamicsb τ1 (ps) τ2 (ps)c 22.9 -37.9 -5.9 28 5.2 93 5.2 294 5.8 912 6.1 2383 5.9 5 5.2 52 5.4 182 5.6 672 6.0 1885 6.8 6732

τ3 (ns) 5.6 -1.3 ----15.2 ------

aFitting

errors were ~0.1 ps and 5-10 ps for τ1 and τ2 respectively, while errors for τ3 tended to be quite large (due to the 8 ns time window). bFitting errors were 0.1-0.3 ps for τ1, errors for τ2 are shown in Figure 4a. cAssociated α2 values were negative to reflect population growth. decay exponentially with distance. The data were fit to eq 2, which relates the charge transfer rate constant kCT to distance, d, and a transmission coefficient, β. 𝑘𝐶𝑇 ∝ 𝑒𝑥𝑝( ―𝛽 ∗ 𝑑)

(2)

Typically, this model is employed for single-step charge transfer44 and has produced related singlestep transmission coefficients of β = 0.7-1.1 Å-1 for charge separation and β = 0.9-1.0 Å-1 for charge recombination in DNA.45-46 Furthermore, these values for the transmission coefficient have been shown to increase with an increasing driving force for charge transfer.46 A transmission coefficient for charge recombination in the NDI-Am-G1 structures was also determined to be β = 1.1 Å-1 (see SI). The β values derived from the data in Figure 4a are about half or a third as large as the reported single step charge transfer values. We posit that this is because hole transport in these systems 17 ACS Paragon Plus Environment


involves multiple (2-3) short distance hops before the hole arrives at Sd. The observed distance dependence also suggests that even the longest of these DNA hairpins are not fully within the incoherent hopping regime, which would result in a power law dependence of rate on distance (𝑘𝐶𝑇 ∝ 𝑑 ―𝜂), with η ~ 2 (corresponding to an effective β ~ 0.1 Å-1 at these distances).21 Furthermore, the A3 structures consistently exhibit faster hole transport times than the A2 structures. This is likely a result of fast (few picoseconds) hole transport to the G-tract in both A2 and A3 structures, coupled with the shorter G-tracts in the A3 structures of the same total length. The charge separation yields were calculated from the maximum amount of Sd•+ generated relative to the original population of 1*NDI. These yields exclude the 25% of photons that excite Sd, so it is not a true quantum yield for charge separation. However, if these hairpins were excited closer to 380 nm (thus excluding Sd absorption) the reported charge separation yields would approach the quantum yields. The charge separation yields are shown in Figure 4b. As expected, the yields decrease with increasing distance but do appear to plateau past six base pairs. This behavior has been observed before and is attributed to a transition from direct transfer (superexchange) to a hopping regime.13, 29 However, the rate constants of hole arrival at Sd suggest that a regime of incoherent hopping is not achieved, and instead hole transport in these longer hairpins likely proceeds via 2-3 hopping steps. The observed plateau in the yield could therefore be derived from the fact that once the holes reach the middle of the G-tract, they will always eventually transfer to Sd. For example, in the NDI-A3-Gn-Sd hairpins, we can assume that ~7-10% of the photoexcited holes are long-lived in the G-tract, and all of these carriers eventually make it to Sd since recombination is blocked by the A-tract. However, a deeper understanding of the charge transfer mechanism in these diblock oligomers would better clarify these experimental observations. For example, applying more sophisticated theoretical frameworks mentioned in the


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introduction (beyond superexchange vs. hopping) involving flickering resonance and delocalized transport could potentially resolve the presence of a plateau in the charge separation yield vs. distance but not in the hole arrival time.

Figure 4. (a) Hole arrival time constants (kSd+) at Sd for (red) NDI-A3Gn-Sd and (black) NDIA2Gn-Sd hairpins with (dashed lines) fits to eq 2 overlain. (b) Charge separation yields for (blue) NDI-A4-Sd, (red) NDI-A3Gn-Sd, and (black) NDI-A2Gn-Sd hairpins. Kinetic Simulations of Charge Transfer in the DNA Hairpins. The dynamics of hole transport in the NDI-Am-Gn and NDI-Am-Gn-Sd hairpins were modeled with kinetic simulations. The dynamics were simulated numerically based on rate constants for hole transfer derived from a previously reported Marcus model for hole transfer in DNA.32 It is worth noting that a similar kinetic model has been reported previously for DNA charge transport in A-tracts.26 This type of kinetic model, though powerful for qualitative understanding, is notably simpler than the recently developed theoretical models for DNA transport that take into account structural fluctuations (flickering resonance),20, 23 coulombic repulsion,21, 23-24 and hot hole states.12 The application of these theories to the diblock systems presented here may help rationalize experimental results not captured by the kinetic model presented below, such as the observation of a plateau in the ion pair 19 ACS Paragon Plus Environment


yield for long hairpins without a corresponding plateau in Sd arrival times indicative of incoherent hopping. Nevertheless, the kinetic model presented here can provide at least a qualitative understanding for the early stages of charge separation and recombination, thus helping us understand why the NDI-A3-Gn-Sd and NDI-A2-Gn-Sd present the same yields for a given length. Furthermore, it provides the first steps towards a more sophisticated model of charge transport in diblock DNA hairpins. To implement the kinetic model, individual charge transfer distances and driving forces were inputted into a Marcus equation for each possible charge transfer step to give approximate rate constants. These rate constants were then incorporated into a numerical kinetic simulation incorporating all possible charge separation and recombination steps in a given hairpin. Individual intermediate states in this kinetic model have the hole localized on a single base or chromophore (delocalization is not explicitly modeled). As the simulations proceed, this hole is allowed to transfer one, two, or three base pairs away at rates that are in accordance with Marcus Theory (distance- and driving force-dependent). Further details of these simulations can be found in the SI. In order to afford qualitatively accurate results in the numerical simulations, one specific rate constant had to be changed significantly (increased) from what the Marcus model would predict: The A-A hopping rate constants. This is justified by two factors. First, adenine polaron formation has been proposed previously to increase the rate of hole transport, which would be reflected in our simple model as fast inter-A hopping. Second, hole transfer from NDI to A-tracts has been shown to create hot holes, which can then transfer to adjacent adenines much faster than isoenergetic hopping.12 The most important time constants used in the kinetic simulation are shown in Scheme 2 for two representative structures. Maximal hole populations on each base are indicated by the area of the associated gray circles. Simulations were performed on all NDI-Am-Gn and NDI-


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Am-Gn-Sd hairpins and accurately reproduce the TA population traces for all sequences, as well as the Sd•+ arrival times for NDI-Am-Gn-Sd hairpins. Comparisons between simulations and experiments are shown in the SI. A

B

Scheme 2. Summary of single step charge separation (red) and recombination (blue) time constants used to construct kinetic models for (A) NDI-AmGn and (B) NDI-AmGn-Sd hairpins, with two representative structures shown. Area of gray circles represent the predicted maximal hole population on an individual site during charge separation. Time constants with asterisks deviated substantially from the time constants predicted by the standard Marcus model. See SI for details. These kinetic simulations can help us understand the distinct dynamics between the A2 and A3 structures. In the A2 structures, the charge separation population diminishes to ~40% within the first 10 ps, and then continues to decay within 100-1000 ps either completely if no Sd is present, or partially if the hole is trapped on Sd (Figure 2b, 3d). This can be understood by looking to Scheme 2a: 40% of the excited hole population makes it to the G-tract since the 3 ps charge recombination competes with the 5 ps charge propagation from the A-tract. Once the hole is at the closest guanine, 150 ps charge recombination competes with charge propagation in the G-tract thus further reducing charge separation yields on the 100-1000 ps time scale. In the A3 structures, 21 ACS Paragon Plus Environment


the charge-separated population quickly diminishes to ~20% within 10 ps, and then stays relatively constant for a few nanoseconds (Figure 3c, and 2b). Scheme 2b clearly shows the origin of this behavior: rapid hole transfer to the G-tract competes with charge recombination such that approximately one fifth of the population makes it to the long-lived G-tract state, from which charge recombination takes ~4 ns. The close correspondence in hole arrival times at Sd between the simulation and experiment justify our use of a 200 ps hopping time between adjacent guanines. Furthermore, this value is consistent with previously reported hopping rates in G-tracts.47 These kinetic simulations provide a qualitative understanding of charge separation and recombination pathways in the presented hairpins. Furthermore, this type of single site Marcus-based kinetic model has features that can simulate both superexchange and hopping regimes since a competition of rates between nearestneighbor hops and charge transfer across multiple bases (superexchange) dictates each step in the simulation. The ability to capture these two experimentally observed regimes makes this kinetic model quite general. The model may neglect more sophisticated nuances of DNA charge transfer such as structural fluctuations (flickering resonance) and charge delocalization or polaron formation, but these features can be approximated (at least qualitatively) with the current model. In order to derive broader lessons from this work, it is worth comparing our results to those found for diblock Sa-AnGm-Sd (stilbenedicarboxamide) hairpins13 and the high-yielding diphenylacetylene hairpins.11 First, the Sa-AnGm-Sd structures presented similar charge separation yields for A2Gm and A3Gm hairpins of the same length, which we can now tentatively understand in terms of the current work that exhibited the same behavior. That is, there are key charge separation/recombination intermediates that dictate charge separation yield: from the A-tract in A3Gm hairpins and the closest guanine in A2Gm hairpins. Second, the identity of the chromophore


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(hole donor) can be revisited. NDI, with a large driving force for charge separation, has a relatively small driving force for recombination (near the Marcus barrierless region). This feature limits the resultant charge separation yields compared to Sa and diphenylacetylene (~30% C.S. yields across six base pairs), which have smaller driving forces for charge separation, but large driving forces for recombination, well in the Marcus inverted region. Although the diblock sequences improve charge separation yields in NDI, using this strategy with new chromophores that present better energetics would result in further improvements. Looking forward, the kinetic simulations presented in this study could be used to screen hypothetical DNA hairpins (both chromophore identity and sequence) to aid in the design of structures with high yield and long-lived charge separation.

CONCLUSIONS We demonstrate the design of high-yield charge separation systems in synthetic DNA hairpins by using diblock oligonucleotides with the hole donating chromophore adjacent to two or three adenines followed by a guanine tract. This architecture serves to promote charge separation to the G-tract and eventually a hole acceptor while retarding charge recombination. A detailed kinetic analysis of the A2 versus A3 structures dissects the relevant charge separation and recombination steps that dictate charge separation efficiency. We find that the critical recombination process occurs from the A-block in the A3 structures, and from the closest G in the A2 structures. Although both A2 and A3 structures exhibit similar efficiencies, kinetic analyses of this type could be used to screen structures with modified nucleobases in designing DNA-based systems for charge separation. ASSOCIATED CONTENT 23 ACS Paragon Plus Environment


Supporting Information UV-Vis and circular dichroism spectra, MALDI mass spectrometry data, calculated free energies for charge transfer, femtosecond transient absorption time-resolved spectra and derived population traces for NDI•- and Sd•+, nanosecond transient absorption single-wavelength traces with kinetic fits, details of the kinetic model including computed time-resolved population traces, and comparisons to experimental data are included in the SI. This material is available free of charge via the Internet at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding Authors [email protected] Notes The authors declare no competing ﬁnancial interest.

ACKNOWLEDGEMENTS This work was supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Award DE-FG02-99ER14999 (M.R.W.) The authors thank Professor Fred Lewis for fruitful discussions and Dr. Itai Schlesinger for assistance with sample preparation.


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Charge Separation and Recombination Pathways in Diblock DNA

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