Interaction of Photogenerated Spin Qubit Pairs with a Third Electron Spin in DNA Hairpins

Article abstract of DOI:10.1021/jacs.0c12645

The designing of tunable molecular systems that can host spin qubits is a promising strategy for advancing the development of quantum information science (QIS) applications. Photogenerated radical pairs are good spin qubit pair (SQP) candidates because th

Full text of DOI:10.1021/jacs.0c12645

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Article
Interaction of Photogenerated Spin Qubit Pairs with a Third Electron
Spin in DNA Hairpins
Emmaline R. Lorenzo,† Jacob H. Olshansky,† Daniel S. D. Abia, Matthew D. Krzyaniak, Ryan M. Young,
and Michael R. Wasielewski*
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ABSTRACT: The designing of tunable molecular systems that can host spin qubits is
a promising strategy for advancing the development of quantum information science
(QIS) applications. Photogenerated radical pairs are good spin qubit pair (SQP)
candidates because they can be initialized in a pure quantum state that exhibits
relatively long coherence times. DNA is a well-studied molecular system that allows for
control of energetics and spatial specificity through careful design and thus serves as a
tunable scaffold on which to control multispin interactions. Here, we examine a series
of DNA hairpins that use naphthalenediimide (NDI) as the hairpin linker.
Photoexcitation of the NDI leads to subnanosecond oxidation of guanine (G) within
the duplex or a stilbenediether (Sd) end-cap to give NDI•−-G•+ or NDI•−-Sd•+ SQPs, respectively. A 2,2,6,6-tetramethylpiperdinyl-
1-oxyl (TEMPO) stable radical is covalently attached to the hairpin at varying distances from the SQP spins. While TEMPO has a
minimal effect on the SQP formation and decay dynamics, EPR spectroscopy indicates that there are significant spin−spin dipolar
interactions between the SQP and TEMPO. We also demonstrate the ability to implement more complex spin manipulations of the
NDI•−-Sd•+-TEMPO system using pulse-EPR techniques, which is important for developing DNA hairpins for QIS applications.
system is desirable for achieving certain quantum computing
benchmarks by providing a means to implement quantum
algorithms.13,21,22
INTRODUCTION
■
An important goal of quantum information science (QIS) is
the search for optimal materials to utilize as quantum bits, or
qubits.1−3 In contrast to classical two-state bits, qubits provide
an exponential increase in computational power and speed that
is promising for vastly expanding computation and other
information technologies.1,4 The design of qubits requires, in
part, that they be initialized in a pure quantum state and have
long coherence times.5 Photogenerated radical pairs are
promising candidates for meeting these criteria because
photoexcitation of an organic chromophore followed by charge
transfer between the chromophore and a neighboring molecule
can result in an entangled spin pair that exists in a pure initial
singlet quantum state (ms = 0).6−12 SQP coherence lifetimes
on the order of microseconds have been demonstrated at
temperatures as high as 85 K, which in some cases is
sufficiently long enough to implement more complex spin
manipulations.13
The scope of SQP functionality and applicability can be
further improved by adding a stable radical to the system as a
third spin qubit.14−19 We have implemented this strategy using
a variety of covalent donor−acceptor-radical (D-A-R•)
triads.7−10,20 The spin−spin interactions between the D•+-
A•‑SQP and R• demonstrate a wide range of phenomena,
including control of the SQP lifetime,7 spin polarization
transfer from the SQP to R•,8,10 spin-selective photoreduction
of R•,9 and quantum teleportation of the R• electron spin
state.20 The ability to control the spin dynamics of a three-spin
While the control and tunability of a three-spin system are
clearly favorable for QIS applications, designing and synthesiz-
ing a variety of D-A-R• systems that have the correct charge
transfer energetics and spin−spin interactions can be difficult.
The ability to easily modify the identity of each component of
a system allows for more rapid progress in producing an
optimal system. The intersection of the more mature field of
charge transfer in synthetic DNA structures and the emerging
search for molecular qubits now offers the possibility to create
an easily modifiable framework that can bear multiple tunable
electron spins.23−26 This goal has precedent in our recent work
that explores photogenerated SQPs in synthetic
DNA.24,25,27−31 Additionally, different facets of electron spin
behavior have been explored in DNA, such as the effect of a
stable radical on DNA structure,32 DNA as a spin filter,33 and
DNA acting as a classical bit.34 Such studies have paved the
way for more complex spin systems to be developed and
implemented in a DNA framework, which will allow for
Received: December 4, 2020
Published: March 18, 2021
https://doi.org/10.1021/jacs.0c12645
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© 2021 American Chemical Society
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Figure 1. (a) The structures of the chromophore/hole donor NDI (green), the terminal hole acceptor, either guanine or Sd (red), and stable
radical, TEMPO (blue). (b) The structure of all DNA hairpins explored in the present work.
Optical Spectroscopy. The femtosecond and nanosecond
transient absorption (TA) instrumentation has been described
previously.42 A brief description of the apparatus and details of the
sample preparation are given in the Supporting Information (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. The buffer for pulse-EPR experiments used 50% D2O
and 50% glycerol-d3 (both 95% d). Samples were photoexcited at 355
nm (7 ns, 10 Hz) from the frequency-tripled output of a Nd:YAG
laser. Experiments were performed at both X-band and Q-band.
X-band measurements. 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 set to 85
K, controlled by an Oxford Instruments CF935 continuous flow
optical cryostat with liquid nitrogen. Solutions (∼10 μL, ∼2 nmol)
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. The samples were prefrozen in liquid
nitrogen before inserting into the precooled instrument. Light from
the pulsed laser was coupled through an optical fiber placed outside
the cryostat window (∼2 mJ/pulse), with some portion of the light
passing through the coils of the resonator and exciting the sample.
Q-band measurements. Measurements were performed on a
laboratory-built Q-band (33.5 GHz) spectrometer described
previously.20 A Bruker Q-band EN 5107D2 resonator was used, and
the sample temperature was maintained at 85 K using an Oxford
Instruments CF935 Cryostat and an ITC503S temperature controller.
Hairpin solutions (∼10 μL, ∼2 nmol) were loaded into quartz tubes
(1.80 mm o.d., 1.50 mm i.d.). The tubes were fitted with a length of
optical fiber (Thorlabs, 0.39 numerical aperture, 1 mm diameter, ∼1
m length, with ∼5−10 cm at the end unprotected by cladding). The
optical fiber was fed through a Bruker sample holder and positioned
so that the fiber was terminated ∼0.5 cm above the top of the sample.
The fiber and quartz tube were sealed together using 2 cm of heat-
shrink tubing. The samples were prefrozen before inserting into the
precooled instrument. The optical fiber was then coupled to a longer
optical fiber that received the output from the pulsed laser (0.3 mJ/
pulse incident on the sample).
exploration of QIS phenomena embedded in a structurally
well-defined system.
Charge transport in DNA occurs primarily by hole transport
between purine bases.35 A wide array of DNA hairpins having
different chromophoric hairpin linkers, base sequences, and
synthetic base pairs have been explored.29,36−39 Upon
photoexcitation of the hairpin linker chromophore, charge
transfer occurs via fast hole injection into an adjacent adenine
and subsequent hole transfer through an A-tract followed by
hole trapping at a guanine or other easy to oxidize molecule
covalently linked to the hairpin as a terminal end-cap. Such
synthetically modified hairpin structures create long-lived
SQPs in large enough quantum yields to be studied with
transient optical and EPR spectroscopies.31,38 A range of
chromophores and terminal end-caps have been shown to
provide different design advantages, like unique energetics and
radical g-factors, allowing favorable spectral resolution.25,29
With the inclusion of an ethynylated uridine nucleobase in the
DNA sequence, a stable radical can be covalently attached with
relative ease and specificity using click chemistry.40,41
In the work presented here, we have designed and
synthesized a series of DNA hairpins to explore the interaction
of a SQP with a stable radical. A naphthalenediimide (NDI,
electron acceptor/hole donor) chromophore is used to
covalently link two single DNA strands to form a DNA
hairpin. Photoexcitation of NDI generates a SQP comprising
NDI•− and a radical cation residing on either guanine or
stilbenediether (Sd) covalently bound as the end-cap on the
sequence (see structures in Figure 1). The 2,2,6,6-tetrame-
thylpiperdinyl-1-oxyl (TEMPO) radical furnishes the third
electron spin and is covalently bound to uridine. The charge
transfer and spin dynamics of these hairpins are benchmarked
against their counterparts without a stable radical using both
transient optical and EPR spectroscopies.
EXPERIMENTAL SECTION
Transient CW EPR. Measurements using continuous wave (CW)
microwaves and direct detection were performed at X-band.
Following photoexcitation, kinetic traces of transient magnetization
under CW microwave irradiation were obtained in both the real and
■
Synthesis. Preparation and characterization of TEMPO deriva-
tives and the DNA hairpins are detailed in the Supporting
Information.
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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.
shown in Scheme 1 was used to attach TEMPO to the 5-
ethynyluracil base.40 The DNA hairpin was then cleaved from
the solid support and subsequently purified by reverse phase
C-18 HPLC. The purity of the hairpins was confirmed via
MALDI-TOF spectroscopy (Table S1) and steady state UV−
vis spectroscopy (Figures S1). In addition, assembly of the
duplexes into B-form DNA was confirmed by circular
dichroism spectroscopy (Figure S2)
Pulse-EPR. Measurements were performed at both X-band and Q-
band. Field swept electron echo experiments were performed at X-
band and Q-band with a 200 ns delay between the laser flash and the
π/2 pulse. At X-band, the π/2 and π pulse lengths were 16 and 32 ns,
respectively, separated by a time τ = 200 ns. The light and dark signals
were collected with separate back-to-back scans, and the difference
between the spectra gave the light-dark (L-D) signal. At Q-band the
π/2 and π pulse lengths were 40 and 80 ns, respectively, separated by
a time τ = 200 ns. A four-step phase cycle was used, and a “dark” pulse
sequence and detection was performed 50 ms after each laser flash
(run at 10 Hz). This allowed for the collection of a light and dark
signal in a single scan. Signals were detected in quadrature and phased
to give absorptive signals (of stable radicals) in the real channel and
derivative signals in the imaginary channel. The dark signal, which
shows the presence of a stable radical impurity, was subtracted from
the light signal to give the photogenerated field swept echo. The echo
was integrated at every field point to give echo intensity vs field. Out-
of-phase electron spin echo envelope modulation (OOP-ESEEM)
experiments were performed at X-band.43−45 The parameters were the
same as the field swept electron echo experiment, except that the time,
τ, was increased incrementally between the π/2 and π pulses.
Charge Transfer Dynamics. The charge transfer dynam-
ics following photoexcitation were explored with TA spectros-
copy to ascertain how the inclusion of TEMPO affects these
dynamics. NDI-A3G1A2 and NDI-A3G1-Sd were used as the
reference hairpins for series 1 and 2, respectively. Following
selective photoexcitation of NDI, the TA spectra (Figures 2,
S3, and S5) all show absorption features characteristic of
NDI•− at 480 and 610 nm, which appear within the ∼300 fs
instrument response function.47 There is no evidence of
48
3
1
significant *NDI formation from *NDI. The features for
the A-tract polaron and G•+ are too weak to spectrally identify
but tracking the time evolution of NDI•− is sufficient to
determine the NDI•−-G•+ lifetimes.49 For structure 2A, the
characteristic Sd•+ radical cation feature at 530 nm was
observed in addition to the same spectral NDI features as seen
in the control hairpin (Figure S5).50
We compare the charge recombination time constants
between the hairpins with and without TEMPO to determine
if its presence alters the SQP dynamics. The charge
recombination lifetimes were determined by fitting the decay
of the NDI•− peak with a triexponential function (Table 1).
The first time constant, τ1 ≅ 3 ps, is assigned to recombination
of the initial contact SQP comprising NDI•− and the
neighboring A•+. The second time constant (τ2) is assigned
to recombination of the delocalized hole within the A-tract,
and the third time constant (τ3) is attributed to recombination
from G•+.31 Comparing these dynamics to the NDI-A3G1A2
control compound for series 1, we observe that charge
recombination occurs on similar time scales for these three
processes. Approximately the same dynamics are observed for
2A and NDI-A3G1-Sd with the addition of a longer
component, τ4, which is assigned to recombination of
NDI•−-Sd•+. The charge recombination time for NDI-A3-G1-
Sd is faster than that of 2A, which may result from structural
distortion of the hairpin caused by the attached TEMPO, as
evidenced by the circular dichroism (Figure S2) and EPR data
(see below). On the basis of the Marcus-Levich-Jortner model,
the charge recombination rate is directly proportional to the
square of the electronic coupling matrix element, which is
affected by structural distortion.47 Thus, even a small change in
coupling can impact the observed charge recombination rates.
Overall, these results demonstrate that the attachment of
TEMPO to the DNA hairpin does not significantly alter the
charge transfer dynamics of the series 1 systems and increases
all the charge recombination times for 2A by less than a factor
of 2. This suggests that any differences observed in the EPR
spectra are due, in large part, to spin dynamics and not
differences in the charge transfer/population dynamics.
RESULTS AND DISCUSSION
■
DNA Hairpin Design. Previous work on the DNA hairpin
NDI-A3G1A2 in Figure 1 has shown that photoexcitation of
NDI with a 355 nm laser pulse leads to hole injection into the
A3 sequence followed by hole trapping at guanine in 20% yield
to produce NDI•−-A3-G1•+-A2, which has slow charge
recombination dynamics.31,39,46 Series 1 is designed to probe
how distance affects the interaction between the spins of the
TEMPO radical and G•+ in the NDI•−-G•+ SQP.31 Series 2
utilizes Sd as the hole acceptor because Sd is much easier to
oxidize than G, leading to higher charge separation yields and
longer SQP lifetimes, which increase EPR signal intensities and
allow for implementation of pulse-EPR techniques.31 The
sequences were synthesized using standard solid-phase
oligonucleotide synthetic procedures (see SI).
In order to incorporate TEMPO into the DNA structure, we
used a postsynthetic modification strategy. A commercially
available synthetic base, 5-ethynyl-2’deoxyuridine (Scheme 1),
was incorporated into the structures during the standard
oligonucleotide synthesis. The click chemistry reaction scheme
Scheme 1. Click Chemistry Reaction Scheme Utilized to
Attach TEMPO to Ethynyluridine, Showing Only the
Nucleobase Involved in the Reaction
Spin Dynamics. We next probed the spin dynamics to see
the effect of the TEMPO electron spin on the SQP in each
structure using several different EPR methods. Continuous
wave (CW) EPR spectroscopy without photoexcitation
confirmed the presence of TEMPO in all hairpins (Figure
S6). Transient continuous wave (TCW) EPR spectroscopy
was used to obtain time-resolved spectra of the photogenerated
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1
Figure 2. (a) TA spectra of NDI-A3G1A2 with the important features of *NDI and NDI•− highlighted, (b) TA spectra of hairpin 1B. (c)
Triexponential kinetic fits (black) at 488 nm for 1A, 1B, 1C, and NDI-A3G1A2.
Table 1. Charge Recombination Time Constants Obtained
from Fitting the TA Spectra with a Triexponential
Function
spectra of both series 1 and 2 show a somewhat distorted e, a,
e, a pattern, due to the fact that NDI•− and G•+ or Sd•+ have
similar g-factors but significantly different spectral widths,
Figure S6. The narrow central features can be assigned to
NDI•−, while the broader features are assigned to either G•+
for series 1 hairpins or Sd•+ for series 2 hairpins.24 The effect of
TEMPO on the NDI•−-G•+ spectra is significant because
additional exchange (JGR) and dipolar (DGR) couplings
resulting from the TEMPO electron spin can broaden the
spectra. However, since JGR depends exponentially on the
distance between the spins, JGR should be negligible because of
the large number of saturated single bonds between the π
system of the neighboring G•+ and TEMPO. In contrast, DGR
∝ 1/r3, where r is the distance between the spins; thus, as
TEMPO is moved closer to G•+ in the SQP, DGR increases.
This increased coupling results in a larger splitting and thus a
broadened spectrum because of the overlap of the NDI•− and
G•+ resonances, which we observe as a qualitative trend for
series 1.
a
Hairpin
τ1 (ps)
τ2(ps)
τ3 (ns)
τ4 (μs)
1A
1B
1C
3.2
3.1
3.3
2.8
2.9
2.7
63
44
38
63
76
67
2.6
2.7
2.6
2.8
17.6
10.4
NDI-A3G1A2
2A
NDI-A3G1-Sd
3.4
2.5
a
For structures with Sd, a fourth longer lifetime component was
obtained. Error bars on kinetic data: τ1 0.4 ps, τ2 10 ps, τ3 = 0.7
ns, and τ4 = 0.1 μs.
SQP. The spectra obtained 100 ns after the laser pulse for each
hairpin are shown in Figures 3a-b, with the corresponding
simulations overlaid in red. On the basis of the spin-correlated
radical pair (SCRP) model,51,52 a photogenerated SQP
produced in an initial singlet state with a positive spin−spin
exchange interaction (J) typically exhibits a spin-polarized e, a,
e, a spectral pattern (e = emission, a = enhanced absorption,
low to high field) arising from two antiphase doublets, each of
which is centered at the g-value of the individual radical. The
Simulations of NDI-A3G1A2 and NDI-A3G1-Sd were
performed using known or calculated values for the g-tensor
24
53
24
and hyperfine couplings of NDI•‑ and G•+ or Sd•+ and
only the relative molecular orientations and the dipolar
couplings were varied. The spin−spin coupling was attributed
Figure 3. TCW spectra (black traces) at 100 ns following a 355 nm, 7 ns laser pulse for (a) series 1 (b) series 2 overlaid with simulated spectra (red
traces).
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solely to dipolar coupling, and the exchange coupling was
assumed to be negligible and was not considered in the
simulations (see SI for details). In order to fit 1A, 1B, 1C, and
2A, a three-spin model was utilized,54 where it is assumed that
TEMPO has net zero polarization relative to the SQP. The full
simulation parameters are provided in Table S2. Due to the
fact that the g-anisotropy, hyperfine anisotropy, and dipolar
coupling are all on the same order of magnitude for
measurements performed at 0.34 T (X-band, 9.6 GHz)55 the
simulations are semiquantitative; however, they do provide
reasonable estimates for the dipolar coupling, so that assuming
the point-dipole approximation,27 they provide the spin−spin
distances and orientations superimposed on the hairpin
structures illustrated in Figure 4. It is important to note that
the DNA hairpin structure of 2A is somewhat distorted by the
combination of placing the U’-TEMPO base at a position
between the NDI hairpin linker and the Sd hole acceptor,
which is linked only to the 5′ strand. This results in a longer
distance between TEMPO and the Sd•+ end-cap.
In order to perform more complex spin manipulations, a
multispin system must be amenable to pulse-EPR experiments.
To this end, the photogenerated SQP in hairpin 2A was
subjected to a Hahn two-pulse echo experiment, π/2-τ−π−τ-
echo, where τ is the delay time between the π/2 and π
microwave pulses at both X- and Q-bands (Figure 5a,b,
respectively).56 The field-swept electron spin echo (ESE)
spectra were recorded before and after photoexcitation and
subtracted to remove the steady-state TEMPO signal. At X-
band, g-anisotropy, hyperfine anisotropy, and dipolar coupling
contribute equally to the observed spectrum, whereas g-
anisotropy dominates at Q-band. The effect of the g-anisotropy
of the nitroxide is more apparent at Q-band, so we observe a
clearer separation of the nitroxide spectrum from the SQP
spectrum, which results in a different spectral appearance of
the light minus dark (L-D) subtracted echo signal. The L-D
subtracted echo signal allows us to observe only the laser-
induced signal, which has little or no contribution from
TEMPO, indicating that there is no spin polarization transfer
to TEMPO or population depletion of G•+ that would result
from oxidation of TEMPO by G•+. Importantly, the interaction
between TEMPO and the spins that constitute the SQP is not
sufficiently strong to hyperpolarize TEMPO in these three-spin
systems. This result points out the need to design DNA
hairpins in which J between one of the spins comprising the
SQP and the stable third spin is sufficiently large to ensure that
the spin entanglement generated by photogeneration of the
SQP can be used to implement quantum operations involving
the third spin.
When the delay time between the π/2 and π microwave
pulses in the Hahn echo experiment performed on a SQP is
scanned, the echo signal from the photogenerated SQP is
phase-shifted relative to that of the same spin system at
thermal equilibrium and appears with the same phase as the
applied microwave pulses.43 Later theoretical studies showed
that this “out-of-phase” (OOP) echo is due to the J and D
spin−spin interactions within the SQP, which modulate the
echo decay as a function of τ, so that the overall observed effect
is termed out-of-phase electron spin echo envelope modulation
(OOP-ESEEM).44,45
Figure 4. Distances obtained from simulation of the TCW EPR
spectra illustrated on the hairpin structures.
The OOP-ESEEM signal obtained from the photogenerated
SQP in 2A is an oscillatory signal on top of an exponential
Figure 5. (a) Light (blue), dark (red), and light-minus-dark (L-D, black) electron spin echo signals for hairpin 2A at X-band and (b) at Q-band.
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Figure 6. (a) Oscillating echo amplitude signal of 2A (red) with exponential fit (black) for phase memory time. (b) Echo amplitude signal with
exponential fit subtracted (red) and fit (black) used to extract distance of SQP.
decay, and a fit to the exponential yielded a phase memory
time Tm = 1.4 μs (Figure 6a), which is on an order of
magnitude that can be used to implement quantum gate
operations.13 Subtracting the exponential fit from the data
separates the oscillatory component in the data, which was
then fit with a function to extract J and D for the SQP (Figure
6b).57 The fit gives J ≅ 0 and using the point-dipole
tailored. The fundamental concepts explored in this initial
study of a three-spin system in DNA point the way toward new
systems that can be employed to implement complex QIS
operations, such as spin state teleportation.
ASSOCIATED CONTENT
* Supporting Information
The Supporting Information is available free of charge at
https://pubs.acs.org/doi/10.1021/jacs.0c12645.
■
sı
approximation,27 yields a spin−spin distance of 23 Å
0.2
Å for the SQP. Our previous work on NDI-Sd hairpins having
the same nominal four base pair length gave a spin−spin
distance of 18.3 Å.24 The larger distance in 2A can be
attributed to a structural distortion of the DNA structure by
the TEMPO-uridine base that is positioned at a site within the
hairpin that is between NDI•− and G•+, which is consistent
with the difference observed in the charge recombination
dynamics for 2A. This structural distortion from TEMPO
could cause the Sd end-cap to rotate away from the hairpin
structure since it is only connected on one side, allowing it
some degree of flexibility. It is also possible that the TEMPO is
distorting the twist of the helix, which could increase the
distance between NDI and Sd. However, it should be noted
that since the OOP-ESEEM data is fit using a two-spin model,
it is also possible that a more sophisticated model is required
to accurately represent the effect of the third spin on the OOP-
ESEEM of the SQP.
Synthesis and characterization, additional optical and
EPR data, and simulation parameters (PDF)
AUTHOR INFORMATION
Corresponding Author
■
Michael R. Wasielewski − Department of Chemistry, Center
for Molecular Quantum Transduction, and Institute for
Sustainability and Energy at Northwestern, Northwestern
University, Evanston, Illinois 60208-3113, United States;
orcid.org/0000-0003-2920-5440; Email: m-
wasielewski@northwestern.edu
Authors
Emmaline R. Lorenzo − Department of Chemistry, Center for
Molecular Quantum Transduction, and Institute for
Sustainability and Energy at Northwestern, Northwestern
University, Evanston, Illinois 60208-3113, United States;
orcid.org/0000-0002-0445-3109
Jacob H. Olshansky − Department of Chemistry, Center for
Molecular Quantum Transduction, and Institute for
Sustainability and Energy at Northwestern, Northwestern
University, Evanston, Illinois 60208-3113, United States;
orcid.org/0000-0003-3658-1487
Daniel S. D. Abia − Department of Chemistry, Center for
Molecular Quantum Transduction, and Institute for
Sustainability and Energy at Northwestern, Northwestern
University, Evanston, Illinois 60208-3113, United States
Matthew D. Krzyaniak − Department of Chemistry, Center for
Molecular Quantum Transduction, and Institute for
Sustainability and Energy at Northwestern, Northwestern
University, Evanston, Illinois 60208-3113, United States;
orcid.org/0000-0002-8761-7323
Ryan M. Young − Department of Chemistry, Center for
Molecular Quantum Transduction, and Institute for
Sustainability and Energy at Northwestern, Northwestern
University, Evanston, Illinois 60208-3113, United States;
orcid.org/0000-0002-5108-0261
CONCLUSIONS
■
We successfully synthesized DNA hairpins that have covalently
linked TEMPO radicals using postsynthetic click chemistry.
Transient optical absorption spectroscopy demonstrates that
TEMPO does not have a significant effect on the charge
injection or recombination dynamics of the photogenerated
NDI•−-G•+ SQP, and only modestly increases the lifetime of
the NDI•−-Sd•+ SQP, most likely due to structural distortion.
In contrast, time-resolved EPR spectroscopy shows that
TEMPO has a distance-dependent effect on the SQP, which
results from dipolar interaction of the TEMPO electron spin
with the SQP. Additionally, field-swept electron spin echo data
show that it is possible to spectrally address just the TEMPO
spin before photogeneration of the radical pair at X-band. At
higher fields such as Q-band or even W-band, TEMPO could
be individually addressed before or after photogeneration of
the radical pair as a result of increased spectral separation due
to g-anisotropy dominating at higher fields. In the future, we
will take a similar design approach that uses a stable radical
that is more strongly exchange coupled to one spin of the SQP
to carry out SQP functions. The tunable architecture of
synthetic DNA allows for easy access to structures in which
spin−spin interactions among multiple spins can be readily
Complete contact information is available at:
https://pubs.acs.org/10.1021/jacs.0c12645
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Article
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Author Contributions
†E.R.L. and J.H.O. contributed equally to this work
Notes
(18) Borovkov, V. I.; Ivanishko, I. S.; Bagryansky, V. A.; Molin, Y. N.
Spin-selective reaction with a third radical destroys spin correlation in
the surviving radical pairs. J. Phys. Chem. A 2013, 117, 1692−1696.
(19) Bagryansky, V. A.; Borovkov, V. I.; Bessmertnykh, A. O.;
Tretyakova, I. S.; Beregovaya, I. V.; Molin, Y. N. Interaction of spin-
correlated radical pair with a third radical: Combined effect of spin-
exchange interaction and spin-selective reaction. J. Chem. Phys. 2019,
151, 224308.
The authors declare no competing financial interest.
ACKNOWLEDGMENTS
■
This work was supported by the National Science Foundation
under grant no. CHE-1900422. E.R.L. was supported by a
National Science Foundation Graduate Research Fellowship
(DGE-1842165).
(20) Rugg, B. K.; Krzyaniak, M. D.; Phelan, B. T.; Ratner, M. A.;
Young, R. M.; Wasielewski, M. R. Photodriven quantum teleportation
of an electron spin state in a covalent donor-acceptor-radical system.
Nat. Chem. 2019, 11, 981−986.
(21) Cao, C.; Han, Y.-H.; Zhang, L.; Fan, L.; Duan, Y.-W.; Zhang, R.
High-fidelity universal quantum controlled gates on electron-spin
qubits in quantum dots inside single-sided optical microcavities.
Advanced Quantum Technologies 2019, 2, 1900081.
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