Photogenerated Spin-Entangled Qubit (Radical) Pairs in DNA

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Photogenerated Spin-Entangled Qubit (Radical) Pairs in DNA Hairpins: Observation of Spin Delocalization and Coherence Jacob H. Olshansky, Matthew D. Krzyaniak, Ryan M. Young, and Michael R. Wasielewski J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.8b13155 • Publication Date (Web): 13 Jan 2019 Downloaded from http://pubs.acs.org on January 13, 2019

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Journal of the American Chemical Society

Photogenerated Spin-Entangled Qubit (Radical) Pairs in DNA Hairpins: Observation of Spin Delocalization and Coherence Jacob H. Olshansky, Matthew D. Krzyaniak, Ryan M. Young, and Michael R. Wasielewski* Department of Chemistry and Institute for Sustainability and Energy at Northwestern Northwestern University, Evanston, IL 60208-3113, USA *[email protected] Abstract The ability to prepare physical qubits in specific initial quantum states is a critical requirement for their use in quantum information science (QIS). Sub-nanosecond photoinduced electron transfer in a structurally well-defined donor-acceptor system can be used to produce an entangled spin qubit (radical) pair in a pure initial singlet state fulfilling this criterion. Synthetic DNA is a promising platform on which to build spin qubit arrays with fixed spatial relationships; therefore, we have prepared a series of DNA hairpins in which naphthalenediimide (NDI) is the chromophore/acceptor hairpin linker, variable length diblock A- and G-tracts are intermediate donors, and a stilbenediether (Sd) is the terminal donor. Photoexcitation of NDI in these DNA hairpins generates high yield, long-lived, entangled spin qubit pairs at 85 K, and time-resolved and pulse electron paramagnetic resonance (EPR) spectroscopies are used to probe their spin dynamics. Specifically, measurements of the distance-dependent dipolar coupling between the two spins is used to obtain the average spin qubit pair distance in the absence of the terminal Sd donor and reveals that one of the spins is fully delocalized across up to five adjacent guanines in a G-tract on the EPR timescale. We have recently shown that extensive spin hopping between degenerate sites accessible to one spin of the pair may result in spin decoherence. However, we observe a strong out-of-phase electron spin echo envelope modulation (OOP-ESEEM) signal from the NDI•- - Sd•+ spin qubit pair in DNA hairpins showing that spin coherence is maintained across a two adenine A-tract followed by a 2-4 guanine G-tract as a result of rapid spin transport to Sd. These results demonstrate that pulse-EPR can manipulate coherent spin states in DNA hairpins, which is essential for quantum gate operations relevant to QIS applications.

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Introduction Research on charge transfer within DNA over the past two decades has focused primarily on understanding biologically relevant DNA function1-4 and the potential use of DNA in molecular electronics.5-7 However, despite the fact that charge transport within DNA is always accompanied by spin transport, there are far fewer studies focused on spin transport within DNA. A notable recent exception has been provided by Naaman and co-workers, who have shown that the helical chirality of DNA allows it to serve as an effective spin filter,8,9 thus expanding the potential applicability of DNA to quantum information science (QIS).10-29 In addition, our group30-33 and that of Majima34,35 have demonstrated that radical pairs (RPs) with initially entangled 2-qubit spin states can be prepared within DNA hairpins by selective photoexcitation of different chromophores incorporated into DNA as either the hairpin linker that joins the two single strands of DNA,31,34,35 as base-pair surrogates at abasic sites within the hairpin,30 or as capping groups appended to the end of the duplex opposite that of the hairpin linker.32,33 These strategies now make it possible to use DNA hairpins to assemble spin qubit arrays with fixed spatial relationships that control the spin-spin exchange (J) and dipolar (D) interactions that result in entanglement. Moreover, subnanosecond photogeneration of an entangled 2-qubit pair in a pure singlet state fulfills a critical requirement for any physical qubit, namely, that it should be capable of being prepared in a welldefined quantum state.36 In principle, these spin qubit pairs can be used to implement quantum gates,10,12,26-29,33,37,38 as well as a means of carrying out spin teleportation.39,40 DNA can also serve as a scalable platform for ultimately being able to uniquely address spin qubits in spatial arrays on surfaces that have been functionalized with DNA in a manner typical of current sensor technologies.41,42 Understanding spin dynamics following spin qubit pair formation in DNA is


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therefore an important first step towards designing quantum gates based on synthetically accessible DNA architectures. Nakatani and Takui have previously explored using DNA as a platform for spin qubits by hydrogen bonding small molecules bearing stable radicals and sequence-specific molecular recognition sites to DNA.43-45 In addition, there are several examples of using two paramagnetic species appended to DNA to measure distances between them using pulse electron-electron double resonance (PELDOR) techniques.46-52 However, neither of these strategies have thus far taken advantage of photoinduced charge transfer to prepare pure entangled 2-qubit states. Previous work on photogenerated RPs in DNA hairpins has used time-resolved EPR (TREPR) spectroscopy,30-34 where the RP is created using a short laser pulse (< 10 ns), and is continuously irradiated with microwaves resonant with the electron spins. This technique has yielded information on the dynamics of singlet-to-triplet interconversion,30,31,34 given approximate geometries of the RP,32 and demonstrated the ability to distinguish between triplet-borne and singlet-borne RPs.32,33 However, the continuous microwave irradiation characteristic of TREPR, although a useful probe of the spin system at early times following the laser pulse, causes ill-defined spin flips that ultimately destroy the initial spin coherence of the system. Furthermore, all systems studied thus far have relatively low RP yields, thus limiting the TREPR signal intensity and reducing the possibility of successfully carrying out more complex pulse-EPR experiments relevant to quantum gate operations. One goal of the work presented here is to prepare and characterize a DNA hairpin structure amenable to pulse-EPR experiments in the solid state at cryogenic temperatures. To achieve this goal, DNA hairpins that achieve high yield, long-lived photogenerated RPs under these conditions were synthesized.



The distance between the spins comprising these photogenerated RPs can be obtained by measuring the dipolar interaction between the two electron spins, which depends on 1/𝑟3, where r is the distance between them. Therefore, when the spins are localized at an oxidized donor and reduced acceptor, the dipolar interaction between the two spins directly gives the distance between them. However, in the case of nearly degenerate donors, such as a G-tract in DNA, the dipolar interaction can also give information on spin hopping, i.e. delocalization on the EPR time scale. We have shown recently that spin hopping between two -stacked electron acceptors within a cyclophane promotes spin decoherence in photogenerated RPs when the hopping rate is comparable to the quantum beat frequency between the coherent spin states.53 Thus, it is important to evaluate both spin delocalization and coherence in RPs generated within DNA systems targeting QIS applications. TREPR data on DNA hairpins using a naphthalenediimide (NDI) chromophore/acceptor as the hairpin linker at 85 K are presented here that provide evidence for spin delocalization along the Gtract in the absence of a terminal hole donor. Additionally, when a stilbene-4,4-diether (Sd) terminal donor end cap is added to the hairpin, the distance between the two entangled spins confined to NDI•- - Sd•+ within the DNA hairpin is determined by out-of-phase electron spin echo envelope modulation (OOP-ESEEM),54-56 a pulse-EPR technique. The observation of strong OOPESEEM shows that spin coherence is maintained in these systems,54-56 and that spin delocalization in the G-tract does not result in significant decoherence. This is most likely a result of rapid spin transfer through the G-tract to Sd. These results also provide specific metrics on the distance between the Sd end cap and the adjacent base pair. Importantly, we demonstrate the feasibility and utility of pulse-EPR in manipulating the coherent RP spin states of DNA hairpins in the solid state


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that are essential for their development into addressable multi-spin qubit arrays capable of performing quantum gate operations relevant to QIS applications.

Experimental DNA

synthesis,

purification,

and

characterization.

The

syntheses

of

bis(2-

hydroxyethyl)stilbene 4,4’-diether (Sd)57 and N,N’-[bis-(3-hydroxypropyl)]-naphthalene-1,4:5,8bis(dicarboximide) (NDI)58 have been described previously, and serve as the diol precursors for preparing their mono-substituted dimethoxytrityl derivatives followed by conversion to their respective cyanoethyl-N,N-diisopropyl phosphoramidites.59 These phosphoramidites were used along with the corresponding phosphoramidites of the four natural DNA nucleosides 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 (confirming that they fold into B-form helices). 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 DNA hairpin concentrations 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,60 and are summarized in the SI. EPR Spectroscopy. All EPR measurements were performed on 200-300 µM solutions of DNA conjugates in 50% aqueous buffer (100 mM sodium chloride and 10 mM sodium phosphate buffer) and 50% glycerol. Deuterated water was used for the pulse-EPR experiments. Solutions were



loaded into quartz tubes (2.40 mm o.d., 2.00 mm i.d.), subjected to three freeze-pump-thaw cycles on a vacuum line (10–4 Torr), and sealed with a hydrogen torch. All EPR measurements were made at X-band (~9.6 GHz) on a Bruker Elexsys E680 X/W EPR spectrometer with a split ring resonator (ER4118X-MS3). The temperature was controlled at 85 K by an Oxford Instruments CF935 continuous flow optical cryostat with liquid nitrogen. Samples were photoexcited at 355 nm (1.5 mJ/pulse, 7 ns, 10 Hz) from the frequency-tripled output of a Nd:YAG laser. TREPR measurements using continuous wave (CW) microwaves and direct detection were performed. Following photoexcitation, kinetic traces of the transient magnetization under CW microwave irradiation were obtained in both the real and imaginary channels (quadrature detection). Time traces were recorded over a range of magnetic fields to give 2D spectra. Spectra were processed by first subtracting the signal prior to the laser pulse for each kinetic trace (at a given magnetic field point), and then subtracting the signal average at off-resonance magnetic field points from the spectra obtained at a given time. Out-of-phase electron spin echo envelope modulation (OOP-ESEEM) measurements were performed by varying the time between an initial π/2 microwave pulse and a subsequent π pulse (16 and 32 ns respectively). The time between these pulses, τ, ranged from 72 ns to 1000 ns in 8 ns increments. The first π/2 microwave pulse was timed to arrive 100 ns after laser excitation, ensuring the maximum RP yield. Full echo signals were collected as a function of τ, and then integrated to give the echo amplitude as a function of τ.

Results and Discussion Structures, energetics, and dynamics. The DNA structures explored in this study are shown in Scheme 1. All structures are DNA hairpins with diblock oligomers containing sequential A and


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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 structures upon photoexcitation of NDI.

G blocks. NDI serves as the hairpin linker and chromophore in these structures. Upon photoexcitation of NDI, ultrafast ( 1 (due to energetic constraints, the spin is not localized within the A-tract after initial charge separation). TREPR studies of the RPs are used to probe site-to-site spin (hole) hopping within the G-tract that is faster than the EPR timescale, and thus appears as spin delocalization. In contrast, the NDI-AmGn-Sd hairpins have localized NDI•- - Sd•+ RP states, and are therefore well-suited for probing the effect of spin transport through the G-tract on the spin coherence of the resultant NDI•- - Sd•+ RP state. The NDIAmGn structures were prepared with at least three adenines, since shorter A-tracts led to 7 ACS Paragon Plus Environment


recombination on timescales faster than EPR measurements can detect. The NDI-AmGn-Sd structures were prepared with two or three adenines in the A-tract to maximize the charge separation yield and therefore the EPR signal intensity. This is informed by our previous work with diblock oligonucleotides composed of A and G tracts using stilbenedicarboxamide (Sa) as the hole donor.62 In that work, conjugates with A-blocks of two or three base pairs adjacent to Gblocks demonstrate 25-30% yields of Sa•- - Sd•+ RPs. Similar yields of NDI•--AmGn-Sd•+ are produced here and the time constant for the formation of the RP having the longest distance (NDI•-A3G4-Sd•+) is < 0.7 ns; thus the terminal RP is born in a singlet state with little or no spin evolution over its formation time. How this affects the propagation of spin coherence in these systems will be discussed below. A more detailed analysis of the sequence dependent yields and charge separation/recombination kinetics for the NDI-AmGn-Sd and NDI-AmGn hairpins is presented in a companion study.63

Figure 1. Transient spectra of DNA conjugates after a 355 nm 60 fs pulse at varying times showing the long-lived RP state that is probed by EPR spectroscopy. a) NDI-A3G3 exhibits spectroscopic features associated with NDI•-. b) NDI-A3G3-Sd exhibits spectroscopic features of NDI•- and Sd•+ in a 1:1 ratio.

Nanosecond transient absorption spectroscopy was used to confirm the identity and lifetime of the photoinduced RP states in these structures. Transient spectra for two exemplar structures are 8 ACS Paragon Plus Environment

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shown in Figure 1. The RP population in the NDI-AmGn structures was monitored via the spectroscopic features of the NDI•- anion as the spectral signature of G•+ is not expected to be visible in these structures.64 The NDI-A3Gn structures exhibit RP lifetimes of 100-400 ns depending on the length of the G-tract, and the NDI-AmG1 structures exhibit highly distancedependent lifetimes ranging from 67 ns to 45 µs for m = 3-5. Therefore, the RP states of both classes of structures have long enough lifetimes to be probed by TREPR spectroscopy. The NDIAmGn-Sd structures also exhibit extended RP lifetimes as observed by the long-lived NDI•- and Sd•+ spectral signatures in the transient spectra (>2 µs). Time traces, time constants, and transient spectra for all hairpins studied are provided in SI. TREPR Spectroscopy. The long-lived RP states achieved in the DNA hairpins described above lend themselves to TREPR and pulse-EPR measurements. In order to obtain pulse-EPR data, it is necessary to immobilize the RP; thus, for ease of comparison, all EPR experiments were performed on frozen solutions at 85 K. It is worth noting that the RP formation rates and yields will be altered at these temperatures. However, G for the initial electron transfer from adenine (A) or guanine (G) to 1*NDI is -1.0 and -1.3 eV, respectively, at room temperature, which still allows G to be strongly negative in frozen solutions, given that low dielectric constants of solid solvents result in ion pair destabilization that can be as much as 0.75 eV.65 This contrasts with DNA hairpins having the corresponding Sa chromophore/acceptor,62 which despite having comparable RP yields at room temperature, do not have sufficiently exergonic G to allow RP formation in frozen solutions. Photogenerated RPs, such as those observed in these DNA hairpins, produce spin-polarized TREPR spectra that can be understood using the spin-correlated RP model.66-69 If the distance between the radicals comprising the RP is large enough that the differences between the local



magnetic interactions of each radical, determined largely by their g-factors and hyperfine

Figure 2. Relative energy levels (not to scale) of the four spin states of a photogenerated RP. The red ellipse indicates the zero-quantum coherence, while the green arrows depict the single-quantum coherences that exhibit allowed microwave transitions.

interactions (a), are on the same order of magnitude as their spin-spin exchange (J) and dipolar (D) interactions, coherent spin evolution mixes the singlet and triplet RP states.67,70-75 Moreover, if the RP is photogenerated from an excited singlet state precursor in a static magnetic field that is large relative to J and D, Zeeman splitting of |T +1〉 and |T ―1〉 away from |T0〉 results in coherent |S⟩ ― |T0〉 mixing to give |ΦA〉 and |ΦB〉 , which are initially populated (Figure 2). The laser pulse that creates the RP generates zero-quantum coherence between |ΦA〉 and |ΦB〉 because ∆ms = 0 for these two states, and thus microwave-induced transitions between them are forbidden.76 The |ΦA〉 and |ΦB〉 mixed states are preferentially populated due to the initial population of the |S⟩ state, so that four allowed microwave-induced transitions can occur between these mixed states and the initially unpopulated |T +1〉 and |T ―1〉 states producing a spin-polarized TREPR spectrum.66,67 The TREPR spectrum consists of two anti-phase doublets, centered at the g-factors of the individual radicals that comprise the pair, in which the splitting of each doublet is determined by J and D.22,73 For example, if J = 0 and D < 0, singlet excited state precursors yield an (e,a,e,a) line pattern, where e = emission and a = enhanced absorption. If the g-factors of the two radicals are similar and are split by hyperfine couplings, the two doublets may overlap strongly, and the 10 ACS Paragon Plus Environment

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signal may appear distorted as is the case for the RPs observed here. Photogenerated RPs have previously been observed and analyzed using the spin-correlated RP model in DNA conjugates.3034

The value of J for the hairpins studied here can be approximated using Marcus parameters,77 and is generally too small to have a major impact on the spectra (see the SI). The g-values for the relevant radicals (NDI•- and Sd•+) are also given in the SI. The value of D can be approximated by the point-dipole approximation: 𝐷=―

3𝜇0𝑔2𝑒 𝛽2𝑒

(1)

8𝜋𝑟3

where µ0, ge, β0, and r are the vacuum permeability, the electron g-value, the Bohr magneton, and the distance between the two spins, respectively, with D = (-2785 mT Å-3)/r3. Since D is distancedependent, we find that it dictates the shape of the spectra for the shortest hairpins studied, but not the longer ones. TREPR spectra were acquired for a series of NDI-Am-Gn structures and were used to assess the degree of spin (hole) delocalization in the G-tract. The structures explored include the NDIA3-Gn hairpins, as well as NDI-A4G1 and NDI-A5G1. The transient spectra collected 100 ns after the laser pulse for NDI-A3G1, NDI-A4G1, and NDI-A5G1 are shown in Figure 3a. There is a clear difference between the shortest NDI-A3G1 hairpin and the other two hairpins. This is a result of the increased dipolar coupling for the shorter distance RP. Therefore, the distance between G•+ and NDI•- is the key determinant of the observed spectrum. Furthermore, the NDI-A3G1 hairpin displays the characteristics of two overlapping ea signals common to RPs. We posit that the broad ea feature is derived from the guanine radical cation (with many electron-nuclear hyperfine interactions), while the central, more narrow, ea feature comes from the NDI radical anion. This large number of hyperfine interactions in the guanine radical cations makes it difficult to perform 11 ACS Paragon Plus Environment


de novo simulations of these NDI-Am-Gn RPs, so precise dipolar coupling values could not be extracted. However, to assess spin delocalization in the G-tract for the NDI-A3-Gn hairpins, we fit these spectra as linear combinations of the NDI•--A3G1•+, NDI•--A4G1•+, and NDI•--A5G1•+ spectra, where the spin is localized on a single G. The relative contributions from these basis spectra

Figure 3. Transient EPR spectra for NDI-AmGn hairpins recorded 100 ns after photoexcitation. (a) Spectra for structures with a single G at varying separations from NDI. (c-f) Spectra for (red) NDIA3Gn hairpins and (black, dashed) simulated spectra composed of single G basis spectra from (a). (b) Percentage of simulated spectra composed of the NDI-A3G1 basis spectrum compared to (dashed line) expected percentages based on full spin delocalization in the G-tract.

should reveal where the spin resides in the G-tract (i.e. how far from NDI•-). The original spectra and fits are shown in Figure 3c-f. There is clearly less NDI-A3G1 character in the spectra as the Gtract increases in length since the spin (hole) can spend more time on guanines further away from the NDI. In fact, if the spectra are normalized such that the NDI-A3G2 spectrum is a 1:1 combination of the NDI-A3G1 and NDI-A4G1 spectra, then the hairpins with longer G-tracts exhibit ratios consistent with full spin (hole) delocalization (Figure 3b). This is not surprising due to the 12 ACS Paragon Plus Environment

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relatively fast 200 ps G-to-G hole hopping rate previously reported.78 See Supporting Information for further details on these fits. TREPR spectra were also obtained for a series of NDI-Am-Gn-Sd hairpins and the results are shown in Figure 4. The NDI•- - Sd•+ RP spectra are qualitatively the same for a given physical separation, as determined by the total number of base pairs between NDI•- and Sd•+. In particular, the EPR spectra for the four base pair hairpins are distinct from the longer hairpins. This effect was determined through simulations not to be an orientation effect resulting from g-value anisotropy but was instead found to be primarily influenced by the value of D. RP simulations were performed using Easyspin,79 using input parameters that included the g-values of Sd•+ and NDI•-, the estimated J values (negligibly small), the RP distance, and the initial |S〉 / |T0〉 population ratios. The spectra are notably distorted from the eaea spectrum expected for spincorrelated RPs. This is due to significant overlap between the four spectral components of the RP simulation since the two radicals have similar g-values with considerable g-anisotropy. These overlapping transitions are shown in the Supporting Information for two exemplar compounds. The RPs from NDI are expected to be solely in the |S〉 spin state since spin-orbit-induced intersystem crossing in NDI is at least an order of magnitude slower than charge separation.80-82 However, there is a possibility for singlet-triplet mixing in the intermediate NDI•--A•+ and NDI•-G•+ RPs before reaching the final NDI•--Sd•+ state. This would result in some population of |T0〉, which can be incorporated into the RP simulation. Simulated spectra that best match the experimental data have a 12-17% |T0〉 population. The longer hairpins are better simulated with larger |T0〉 populations, likely due to the longer time available for singlet-triplet mixing to occur in the intermediate NDI•--A•+ and NDI•--G•+ RPs prior to formation of the final NDI•--Sd•+ state.



Figure 4. Transient EPR spectra for NDI-AmGn-Sd hairpins recorded 100 ns after photoexcitation. (ab) NDI-Am-Sd hairpins, (c-d) NDI-A2Gn-Sd hairpins, and (e-h) NDI-A3Gn-Sd hairpins. (red) Experimental and (black, dashed) simulated spectra are overlain.

The other free parameter in these simulations is the RP distance because it affects D. For the hairpins with 5-7 base pairs, this parameter is unimportant because D is smaller than the linewidth. However, for the four base pair hairpins, a RP separation of 16.2 Å was deduced. This is slightly less than the 17 Å expected separation based on standard DNA stacking separations. However, it should be noted that these simulations have too many free parameters to serve as true fits to the data; they instead provide a qualitative picture of the RP distances in these hairpins. Notably, they first demonstrate that the RP spectrum is not significantly affected by the identity of the DNA base pairs between the two molecules on which the radicals reside. Secondly, the RP spatial separation 14 ACS Paragon Plus Environment

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significantly alters the TREPR spectrum only for hairpins that are short enough to have D greater or equal to the spectral linewidth. OOP-ESEEM. Electron spin echo envelope modulation (ESEEM) is a pulse-EPR technique that can give the values of perturbative energy spacings on a simple two-level system, read out as the frequency of the spin echo modulation.56 In ESEEM spectra of stable radicals, these perturbative energy gaps derive from hyperfine splittings and result in characteristic frequencies associated with different nuclei. When ESEEM is performed on spin-correlated RPs, the echo appears “outof-phase,” i.e. in the detection channel in quadrature to the one in which it is expected, and is therefore termed OOP-ESEEM.54-56 The relevant perturbative energy spacing in OOP-ESEEM is the |S〉 ― |T0〉 energy gap, which depends on J and D. If J is small (as it is in the hairpins studied here), then the energy gap is approximately 2D/3, which will directly correspond to oscillation frequencies in the OOP-ESEEM. Since D is related to RP distance in a reliable manner (eq 1), OOP-ESEEM serves as a means to measure this distance. This technique has been used to measure RP distances in photosynthetic reaction centers,83,84 and in donor-acceptor molecules used for artificial photosynthesis.85 More importantly, the observation of strong OOP-ESEEM shows that spin coherence is maintained in the RP.54-56 Therefore, in the case of the DNA hairpins studied here, it can serve as a probe of whether significant spin decoherence has occurred in moving one of the spins through the G-tract to Sd. OOP-ESEEM was performed on NDI-Sd hairpins with 4-6 base pairs (NDI-A2G2-Sd, NDIA2G3-Sd, and NDI-A2G4-Sd), and the results are shown in Figure 5. Full echos were collected as a function of the time between pulses (τ) and are shown in the SI. The data in Figure 5 show the integrated echo intensities as a function of τ, and clearly demonstrate a trend based on number of base pairs. With decreasing hairpin length, the NDI•--Sd•+ distance decreases and D increases (eq



1), which results in the observed higher frequency oscillations for the shortest hairpin. The data were simulated using a previously reported model,83 which relies on D and J. Since J is negligible, the primary free parameter is D. The values of D were then used with eq 1 to determine the RP distances given in Figure 5. The strong OOP-ESEEM oscillations observed for NDI-A2G2-Sd, NDI-A2G3-Sd, and NDIA2G4-Sd show that significant spin decoherence does not occur as the spin traverses up to 6 base pairs before localizing on Sd. Moreover, any tendency for the spin to delocalize amongst the guanines in the G-tract does not destroy spin coherence. This is most likely a consequence of rapid spin (hole) transport through the intervening base pairs, which in all cases occurs faster than 0.7 ns, and is thus faster than spin evolution caused by either electron-nuclear hyperfine interactions or environmental influences at 85 K.

Figure 5. OOP-ESEEM for NDI-A2Gn-Sd hairpins. a) Experimental data for NDI-A2G2-Sd (red), NDIA2G3-Sd (blue), and NDI-A2G4-Sd (green). Simulated echo modulations (black) used to predict the RP distances listed for each hairpin based on the extracted dipolar coupling constant. b) Cartoon of NDI-A2G2-Sd illustrating the rotation of the Sd end cap necessary to achieve the measured RP distances between NDI•-and Sd•+.


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An interesting aspect of the DNA hairpin structure can also be determined from the OOPESEEM data. The data shows that increasing the number of base pairs, on average, increases the RP distance by 3.25 Å. This is consistent with the ~3.3Å base-pair separation expected for similar B-form DNA hairpins.86 However, if the distance between each base pair is ~3.3 Å, and the NDI hairpin linker is locked in place adjacent to the nearest A-T base pair (the NDI-DNA distance is likely ~3.4-3.5 Å), this would imply that Sd•+ is on average 4.6-5.0 Å from the adjacent DNA base pair. The Sd end cap is only linked to the DNA on one side, so some flexibility in its location is expected. To quantify the degree of Sd rotation away from the adjacent base pair, the Sd geometry from a reported DNA hairpin crystal structure in which Sd served as the hairpin linker was consulted (see SI).86 These metrics, coupled with the 4.6-5.0 Å distance between Sd and nearest base pair, suggest that the Sd is rotated from the rest of the DNA hairpin on average by about 10°. It should be noted that the distances shown in Figure 5 are for the simulated traces that best match the data and are subject to 0.1-0.2 Å uncertainty. The OOP-ESEEM data therefore affords information about the preservation of spin coherence during spin transport through a series of base pairs, as well as the RP distances in these synthetic DNA hairpins. Given these advantages, this technique could be used to probe both the structure and coherence of RPs in more complex oligonucleotide structures such as i-motif DNA87 and three-way junctions.88 Conclusions Selective photoexcitation of NDI in the DNA hairpins presented here results in efficient RP formation in frozen solution at 85 K. The TREPR spectra of the RPs show distinct features associated with distance-dependent dipolar coupling, which is used to show that full spin delocalization on the EPR timescale occurs along the G-tract when the Sd end cap is not present.



Additionally, when the Sd end cap is present, OOP-ESEEM is used to show that spin transport across as many as 6 base pairs is fast enough relative to spin evolution in these RPs to result in a spin coherent terminal RP in which the two spins are localized at NDI and Sd. In addition, the RP distance data obtained on the NDI-linked hairpins with Sd end caps shows that the Sd end cap is not cofacial with the last base pair but is instead rotated about 10° away from the base pair. These results highlight the feasibility of using pulse-EPR to probe spin coherence of RPs that can function as qubit pairs in DNA systems and represent an initial step towards more precise control of spin states in DNA for QIS applications. ASSOCIATED CONTENT Supporting Information UV-Vis and circular dichroism spectra. MALDI mass spectrometry data, nanosecond transient absorption spectroscopy data, predicted values for J and D, electronic g-values for NDI•- and Sd•+, spin delocalization fitting parameters, SCRP simulations, OOP-ESEEM full spin echoes, and the geometry of the Sd end cap derived from OOP-ESEEM measurements are included within 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


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Photogenerated Spin-Entangled Qubit (Radical) Pairs in DNA

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