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Temperature Dependence of Electrochemical DNA Charge Transport: Influence of a Mismatch Chris H. Wohlgamuth, Marc A. McWilliams, and Jason D. Slinker* Department of Physics, The University of Texas at Dallas, 800 West Campbell Road, Richardson, Texas 75080, United States S Supporting Information *

ABSTRACT: Charge transfer through DNA is of interest as DNA is both the quintessential biomolecule of all living organisms and a self-organizing element in bioelectronic circuits and sensing applications. Here, we report the temperature-dependent properties of DNA charge transport in an electronically relevant arrangement of DNA monolayers on gold under biologically relevant conditions, and we track the effects of incorporating a CA single base pair mismatch. Charge transfer (CT) through double stranded, 17mer monolayers was monitored by following the yield of electrochemical reduction of a Nile blue redox probe conjugated to a modified thymine. Analysis with cyclic voltammetry and square wave voltammetry shows that DNA CT increases significantly with temperature, indicative of more DNA bridges becoming active for transport. The mismatch was found to attenuate DNA CT at lower temperatures, but the effect of the mismatch diminished as temperature was increased. Voltammograms were analyzed to extract the electron transfer rate k0, the electron transfer coefficient α, and the redox-active surface coverage Γ*. Arrhenius behavior was observed, with activation energies of 100 meV for electron transfer through wellmatched DNA. Single CA mismatches increased the activation energy by 60 meV. These results have clear implications for sensing applications and are evaluated with respect to the prominent models of DNA CT.

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and enzymatic activity.23−26 Unlike photoexcitation experiments, ground state electron transfer is probed. Prior electrochemical experiments have established that DNA charge transport proceeds through the bases and not the sugar phosphate backbone.43 Redox activity strongly depends on the electronic coupling of the probe to the base pair π-stack.44 Recent work has shown that charge transport through DNA monolayers is efficient through 100 base pairs.26 However, the precise charge transport mechanisms have yet to be fully elucidated. Studying the temperature dependence of molecular charge transport processes is of vital importance for clarifying the dominant transfer mechanisms, but a full characterization of DNA-mediated electrochemistry with temperature has yet to be reported. Others have reported temperature-dependent measurements of the conductivity of DNA suspended between

harge transport through DNA is of both fundamental and practical interest. Fundamentally, DNA has a unique configuration of π-stacked bases in a well-ordered, double helical structure. Given its unparalleled importance to life processes and its arrangement of conjugated subunits, DNA has been a compelling target of conductivity studies.1−20 Practically, the charge transport properties of DNA are now being exploited to sense biological targets and to probe biological activity.21−26 Furthermore, given that DNA can self-assemble into hierarchical nanoscale structures,27−30 it is of interest for use in molecular electrical circuits. As a method of studying charge transport through DNA by purely electrochemical means and to facilitate label-free detection of biological targets, DNA-mediated electrochemistry was pioneered.6,21−23,25,26,31−42 DNA is self-assembled as a monolayer on an electrode surface via a synthetic linker, and a redox reporter is inserted into or attached to the DNA to probe charge transfer through the DNA base pair π-stack. The sensitivity of DNA electrochemistry to the structure of the base-pair π-stack has been utilized to sense single-nucleotide polymorphisms,6,21,25,26,42 base lesions,35 proteins,22,23,32,34,36,39 © 2012 American Chemical Society

Received: August 30, 2012 Accepted: December 20, 2012 Published: December 20, 2012 1462

dx.doi.org/10.1021/ac302508f | Anal. Chem. 2013, 85, 1462−1467

Analytical Chemistry

Article

Figure 1. Illustration of the chip layout for studying self-assembled monolayers of probe-modified DNA on multiplexed gold electrodes.

carbon alkanethiol linker on the 5′ end of one strand for selfassembly on gold electrodes. The distal end of the DNA duplex was modified with a Nile blue redox probe.22 We used Nile blue because it is covalently coupled and electrically conjugated to a modified thymine (see Supporting Information). Thus, the redox probe is in a definite position on the DNA duplex with electronic coupling to the base pair π-stack. Efficient electronic coupling of the probe is critically important to DNA electrochemistry.44 The well-matched monolayer used in this study was the 17mer sequence 3′-CTCTATATTTCGTGCG(TNB)-5′ hybridized with the fully complementary sequence 5′(C6 thiol)-GAGATATAAAGCACGCA-3′, where TNB is the Nile blue modified thymine, and C6 thiol is a 6-carbon alkanethiol. The base T also notes the location of the C for the CA single base pair mismatch sequence. Thiolated sequences were obtained from Integrated DNA Technologies (IDT), while the DNA containing the Nile blue precursor base was purchased from Trilink and the dye covalently coupled. These DNA sequences were each doubly purified by high performance liquid chromatography (HPLC) and ethanol precipitated for buffer exchange. The products were characterized by HPLC, matrix assisted laser desorption ionization time-of-flight mass spectrometry, and UV−visible spectrophotometry. Precise details on the probe coupling chemistry and purification steps can be found in other works.22,25 As shown in Figure 1, the DNA films were assembled on chips bearing 16 multiplexed electrodes that permit interrogation of four sequences on each chip with 4-fold redundancy. Electrodes were backfilled with mercaptohexanol to prevent direct interaction of the DNA with the electrode surface. The DNA monolayers were maintained in phosphate buffer (5 mM monobasic/dibasic sodium phosphate at pH 7, 50 mM sodium chloride, 4 mM spermadine) throughout assembly and electrochemical testing. The chips were fabricated in a cleanroom environment and UV−Ozone treated to remove organic contaminants. This chip arrangement also enabled clear comparison between molecular monolayers, as each electrode surface on a given chip was subject to the same processing and cleaning history. The chip system also ensures temperature uniformity across the monolayers, and all results are obtained over averages of multiple monolayers. The chips were connected to electrochemical testing hardware (CH Instruments CHI750D Electrochemical Analyzer and CHI 684 Multiplexer) via a custom mount. Temperature control was achieved by placing this entire mount in a custom copper enclosure and submerging this conglomerate assembly in a temperature controlled, recirculating water bath (See Supporting Information Figure 1). Ruthenium hexamine for surface coverage quantification was purchased from Strem Chemical. Details of chip preparation and DNA assembly may be found in our earlier work.25

electrode gaps. Yoo et al. focused on electrical measurements of poly dG/dC and poly dA/dT sequences from ∼50 K to room temperature.45 Conductance was found to be highest at higher temperatures, with dG/dC sequences showing considerably higher conductance than dA/dT sequences. Interestingly, the dG/dC DNA was found to behave as a p-type semiconductor, while the dA/dT sequence exhibited n-type behavior. Kasumov et al. observed very shallow temperature dependence of electrical transport, with conductivities slightly decreasing with temperature down to 1 K and with resistance on the order of 100 kΩ per molecule.46 Iqbal et al. followed the conductivity of an 18-mer DNA sequence through the melting transition by temperature cycling between 300 to 400 K.47 This heat cycle caused a large decrease in the observed current because of the denaturing of the double-stranded sequences. Notably, all of these results were collected on dry DNA samples and not under biologically relevant conditions, in buffer solution at physiological pH near biologically relevant temperatures. These conditions are important to maintain for both significance to life processes and biosensor applications. Nor has the effect of single-base mismatches been investigated in a temperature-controlled environment. The difficulty in measuring DNA electrochemistry under physiological conditions arises in controlling the uniformity of the temperature of the electrode-bound monolayer and the surrounding solution environment. It is necessary to maintain the DNA in solution under physiological conditions to preserve hybridization and the double helical structure, thus ensuring biological relevance. We have designed and constructed a chipbased system through which we can study multiple DNA monolayers with redundancy in a temperature-controlled environment (see Supporting Information). This setup enables high fidelity measurements of transport dynamics over multiple electrodes and DNA sequences. Here we report the temperature-dependent properties of DNA charge transport in an electronically relevant arrangement of DNA monolayers on gold. We specifically investigate the temperature dependence of the electrochemical reduction of a DNA-bound redox probe and elucidate the role of the DNA bridge. In addition to fully well-matched double stranded DNA, we characterize the influence of a CA single base pair mismatch on DNA CT. The results provide valuable fundamental insight into the CT process and inform design of electrical and electrochemical devices. Our results are also discussed within the context of the prominent CT models.

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EXPERIMENTAL SECTION Figure 1 illustrates the monolayers and the platform used for interrogating the temperature dependence of DNA CT and making comparisons between distinct DNA sequences. The double stranded DNA monolayers were prepared with a 61463



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RESULTS AND DISCUSSION Figure 2 shows an example of the 0−41 °C behavior of the cyclic voltammetry (CV) and square wave voltammetry (SWV)

Figure 2. Cyclic (left) and square wave (right) voltammograms from a well-matched 17mer DNA monolayer modified with a Nile blue redox probe, averaged over a single chip.

Figure 3. (Upper) Logarithmic plot of square wave voltammetry (SWV) peak current versus temperature for well-matched (WM) and single CA mismatch (MM) DNA monolayers, each averaged over 5 chips and 40 DNA monolayers. Error bars represent the standard error of the mean for each point. (Lower) The ratio of well-matched to mismatch SWV peak current with temperature over these chips.

of well-matched, Nile blue-modified 17mer DNA monolayers on 2 mm2 gold electrodes. As noted above for these sequences, the redox probe is located at the top of the duplexcompletely distal to the electrode. The peaks in the CV (50 mV/s) and SWV (15 Hz) are characteristic of the reduction of the Nile blue probe.22,25 The height of these peaks is proportional to the total charge that reaches the Nile blue probes, so this is considered a measure of total transport through the DNA. At low temperature, the CV peaks are small and difficult to quantify, so we use SWV peak current to obtain the yield of total charge transport, as it is more sensitive to the surface bound peak.48,49 The Nile blue redox peaks proceed from very small at 0 °C and increase dramatically in height up to 41 °C. In addition, the splitting between oxidative and reductive CV peaks decreases with temperature, indicative of faster kinetics. These dynamics contribute to the increase of SWV peak current with temperature, as seen in Figure 2. Beyond these temperatures, this double stranded 17mer melts (TM = 64 °C in PO4/ spermidine buffer), and the signals drop dramatically as the Nile blue strand is no longer fully hybridized to its complementary, electrode-bound strand. These dynamics are summarized in Figure 3, which shows the SWV peak current averaged over all the monolayers of this study on a logarithmic plot as a function of temperature. For the well-matched (WM) monolayers, the current increases by nearly a factor of 10 from 0 to 41 °C, and the behavior is best fit by exponential growth. Also shown in Figure 3 is the SWV peak current from monolayers containing a single mismatched base pair (MM): a CA mismatch located near the center of the sequence (TM = 56 °C in PO4/spermidine buffer). For low temperatures and near room temperature, the peak currents are smaller for the mismatch-containing monolayer, consistent with many reports of this effect at room temperature.6,21,25,26,42 However, the mismatched monolayers exhibit a more pronounced exponential increase in peak current with temperature, such that the ratio of peak currents, WM/MM, decreases dramatically and approaches one. These trends and features are also present in the CV currents (see Supporting Information). This is similar to the solution-based temperature dependent yield of DNA-facilitated fluorescence quenching over four bases as reported by O’Neill et al.50 Interestingly, although the presence of a mismatch attenuates DNA CT, higher temperatures “repair” the effect of the mismatch.

To verify that the differences in WM and MM monolayers were not due to differences in surface assembly, we checked the redox signal of these monolayers in the presence of ruthenium hexamine, a groove binder that effectively reports differences in assembly coverages.51 These signals were consistently found to be the same (see Supporting Information) in spite of the observation of differences in probe signals. Thus, our mismatch dependence is not simply a matter of differences in surface coverage, consistent with previous results from Kelley et al.42 These results provide insight on biosensor and electronic device operation. For sensing genetic fragments and single nucleotide polymorphism targets, DNA CT discrimination is greatest at low temperature. This is advantageous, as hybridization of targets is also enhanced with cooling. Protein and enzymatic sensing by DNA-mediated electrochemistry is assisted by larger absolute signals as would be achieved at higher temperatures. This is advantageous for sensing proteins in living systems at physiologically relevant temperatures near 37 °C. Concerning general electronics, our results indicate an energetic barrier is present in the process, and mismatched bases increase this barrier. A conclusive identity of this barrier will assist subsequent device fabrication. Along these lines, we have obtained the temperature dependence of several key kinetic parameters for each DNA monolayer with the method presented by Osteryoung and coworkers.52 The details of this method are provided in the Supporting Information. Using this method, we extracted the electron transfer rate k0, the electron transfer coefficient α, and the redox active surface coverage Γ*, which are plotted in Figure 5 over all chips of this study. The transfer coefficient α is only weakly temperature dependent. The transfer rate k0 increases by a factor of 2 from 0 to 35 °C for the wellmatched monolayer, similar to ferrocene alkanethiol monolayers on gold.53 For many systems, the coverage factor Γ* reports the static absolute coverage of the surface-bound redox species, but for these monolayers, Γ* is strongly temperature dependent, increasing by a factor of 3 over this temperature range. Thus, for our system, Γ* is a dynamic factor that returns not the absolute surface coverage, but rather the redox-active 1464



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Figure 4. Illustration of the increase of electrochemically active DNA with temperature for well-matched DNA monolayers. At low temperature, many duplexes are not in a CT-active state (red), but increased temperature increases the number of DNA duplexes capable of supporting charge transport (green).

Figure 5. Electron transfer rate k0, electron transfer coefficient α, and redox active DNA surface coverage Γ* versus temperature for well-matched (WM) and single CA mismatch (MM) DNA monolayers, each averaged over 5 chips and 40 DNA monolayers. Also plotted with Γ*, the square wave peak current is shown as solid lines to show the correlation.

sequence exhibited activation energies of 105 and 166 meV, respectively. Thus differential kinetics accounts for at least some of the mismatch ratio dynamics noted in the CT yields. The Arrhenius behavior of DNA CT has not yet been observed for DNA electrochemistry or electrical configurations under biologically relevant conditions. The difference in temperature dependence of the redox activity for well-matched versus mismatch-containing monolayers indicates that the dominating factor in the activation behavior is the composition of the DNA bridge itself. In further support of this, changing the linker from a 6-carbon to a 9-carbon linker does not appreciably change the temperature dependence (see Supporting Information). The observation of monotonic activation behavior for both well-matched and mismatch-containing DNA monolayers differs from that of the solution-based temperature study by O’Neill et al.50 Thus, it would appear that some feature of the electrochemical configuration is contributing to distinct CT dynamics, be that in the details of the surface coupling or morphology, the redox probe, or the ground state dynamics. Several mechanisms have been introduced to explain the features of DNA-bound probe electrochemistry. Some have argued that direct interaction of the probe with the electrode accounts for the redox chemistry of DNA systems. Anne et al., investigating ferrocene-modified DNA monolayers on gold, argued that the flexibility of the duplex allows direct interaction of the redox probe with the surface, and others have argued a similar mechanism with this probe.54−56 However, ferrocene probes are oxidized at positive potentials versus Ag/AgCl electrodes, whereas the Nile blue probe is reduced at negative potentials, where the sugar phosphate backbone of the DNA is repelled from the surface.57 Other studies using reductive methylene blue58 or Nile blue59 have suggested direct surface interaction, but these papers primarily concern single-stranded DNA58 or assemblies with long, flexible probe linkers.59 Notably, our constructs are double-stranded duplexes with a

surface coverage of our monolayers. It can be seen in Figure 3 that the square wave peak current tracks Γ*, as it should. Alternatively, we estimated the surface coverage on our chips using a probe bound at the bottom of the duplex25 (not involving DNA CT) to be approximately 20 pmol/cm2. This surface coverage is similar to that found for radioactively labeled, densely packed monolayers by Boon et al.23 Thus, Γ* is approximately a factor of 10 lower than the absolute surface coverage of DNA. That is, it appears that only a fraction of each monolayer is electrochemically reduced, about 10% at room temperature. So we label Γ* as a redox active surface coverage factor. While the transfer rate for the mismatched sequence is marginally higher for high temperatures, the redox active surface coverage is consistently lower, indicating less overall ordering of the bases across the monolayer. In Figure 6, we show the results of plotting the natural log of the electron transfer rate k0 against inverse temperature, and clear Arrhenius behavior is observed for well-matched and CA mismatch monolayers. The slope is more pronounced for the mismatched monolayer, indicating greater activation energy for charge transport. Precisely, the well-matched and CA mismatch

Figure 6. Natural logarithm of the electron transfer rate versus inverse temperature for well-matched (WM) and single CA mismatch (MM) DNA monolayers, averaged over 5 chips and 40 monolayers. 1465



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the integrity of the DNA base pair π-stack. In addition, the CT yield increases dramatically with temperature, indicative of more DNA bridges becoming active for charge transport. These results provide insight for electrochemical biological sensing and fundamental kinetic parameters of DNA CT under biologically active, device-relevant conditions.

short, conjugated probe linker tested under buffer conditions and potentials similar to those of an electrochemical AFM study showing DNA to orient perpendicularly to the electrode surface.57 In direct collision electrochemistry, mismatch dependence has been correlated with a factor of 2−4 difference in electron transfer ratedifferences in redox yields amount to finding a voltammetry frequency that maximizes this rate difference.56 In our work, the WM and MM monolayer transfer rates differ by at most 20%, yet significant mismatch dependence exists in the yields of CT. Also, the roomtemperature transfer rates of direct collision electrochemistry are typically orders of magnitude higher26,55,56,58,59 than the ∼2 electrons/s noted here, a value that is consistent with ratelimited tunneling through the alkanethiol linker.37 We do not see any secondary high transfer rate peaks indicative of a second transport mode.59 The dense films used in this study and observation of mismatch dependence are consistent with DNA-mediated transport regimes.59 So it is our understanding that these signals are indeed DNA-mediated. Nonetheless, DNA conformation and flexibility may play a significant role as ordering of the stack enhances CT, and disorder results in loss of CT.60−62 As low temperatures completely suppress DNA CT, evident by the trend here and shown by previous photoluminescence quenching experiments,62 the equilibrium conformation of DNA is not CT active, and thus a thermally assisted conformational change is necessary. The smooth transitions in yield with temperature would imply a continuum of conformational states are present, only some of which facilitate CT. Flexibility may indeed be the cause of the mismatch dependence of the redox yields, not by enabling direct transfer with the electrode, but rather by disabling DNA-mediated CT to a greater degree in the case of the more flexible mismatch-containing sequence. Thus, direct probe reduction is insufficient to account for our observations. Likewise, conductivity by virtue of ions as opposed to through the DNA bases is excluded on the sensitivity of the conductivity to mismatches and lack of sensitivity to removal of charged phosphate backbone segments.43 Of more plausibility then are tunneling and hopping mechanisms of transport through the DNA bridge. The observation of thermal activation of CT is suggestive of hopping transport, though the length dependence of the rate of electron transfer is also key to establishing this mechanism.63,64 We are currently working on experiments to this end. Thermally assisted tunneling through the DNA may also contribute. The energetic levels of organic molecules can be strongly temperature-dependent, particularly in cases such as this where π-conjugation is possible.65

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ASSOCIATED CONTENT

S Supporting Information *

Images of the custom temperature controlled electrochemical setup, chemical drawings of the C6 linker and Nile blue redox probe coupling, melting curves of well-matched and mismatched DNA, data for the CV analog of Figure 3, DNA voltammetry in the presence and absence of ruthenium hexamine, details of simulations for obtaining kinetic parameters, and temperature dependence of DNA voltammetry with various linkers. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Fax: 972-883-2848. Author Contributions

The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors are grateful for fruitful discussions with Jacqueline Barton and Rudy Marcus of Caltech, Joey Genereux of the Scripps Institute, and Yuri Gartstein of UT Dallas. The authors also thank David Taylor for assistance in design and construction of the experimental setup. This work was performed in part at the UT Dallas Cleanroom Research Laboratory.

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ABBREVIATIONS CV cyclic voltammetry SWV square wave voltammetry WM well-matched DNA sequence MM mismatched DNA sequence HPLC high performance liquid chromatography TM melting temperature

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CONCLUSIONS Charge transfer through surface-bound DNA monolayers is shown to be strongly temperature dependent. Mismatches are found to attenuate transport most at low temperature, but the effect of a mismatch is diminished as the temperature approaches the melting transition. Our results indicate that electrochemical sensing of genetic fragments will be most selective toward single base mismatches at low temperatures. Protein sensing is augmented at high temperatures, where absolute signals are maximized. Kinetic analysis revealed Arrhenius behavior, with activation energies near 100 meV for fully well-matched 17mers. Single base CA mismatches are shown to increase the activation energies by 60 meV, demonstrating that the activation barrier is associated with

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