Resolving the Mystery of the Elusive Peak: Negative Differential

LETTER pubs.acs.org/JPCL

Resolving the Mystery of the Elusive Peak: Negative Differential Resistance in Redox Proteins Elad D. Mentovich,†,‡ Bogdan Belgorodsky,† and Shachar Richter*,†,‡ † ‡

School of Chemistry, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel University Center for Nanoscience and Nanotechnology, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel

bS Supporting Information ABSTRACT: Vertical molecular transistors are used to explain the nonconformal electron transfer results obtained for redox proteins. The transport characteristics of a negative differential resistance peak as appears in the transport data of azurin and its nonredox derivative are explored. A correlation between the peak and its redox center is demonstrated. SECTION: Electron Transport, Optical and Electronic Devices, Hard Matter

S

ince the proposal of Aviram and Ratner almost four decades ago to exploit molecules as electrical rectifiers, numerous theoretical and experimental works have been performed to develop this concept by investigating the nature of electron transport (ET) through diverse types of molecular junctions (MJs).1 The basic structure of an MJ consists of two metallic leads coupled to a single molecule or molecular film. The ET properties of the MJ are commonly explored by utilizing current versus voltage (I/V) characteristics. Practically, several types of MJs have been demonstrated, such as break1 and nanocavity junctions,2 soft-lithography-based devices, and scanning-probebased junctions. However, although much transport data has been acquired during the past few years, conformal results have not been obtained, a fact that seriously limits the understanding of the MJ concept. Surprisingly, it has been found that the charge-transfer characteristics of similar molecular compounds often varied dramatically when measured with different experimental tools. It was previously pointed out that the main reasons for these inconsistencies were the large differences in the conditions and experimental parameters, which vary among various methodologies.3 Some examples of such parameters are conformational configurations, surface and molecular defects, coupling strength, and interfaces between the molecule and the MJ leads.4,5 In this context, the use of a molecular transistor (MT) for ET measurements offers some advantages over other techniques. In an “ideal” MT, a third gate electrode is introduced and used both for tuning the potential drop that falls on the measured molecule(s) and modulating the available energy levels within the Fermi window (Figure 1). Recently, Song et al.6 showed that under the application of an r 2011 American Chemical Society

Figure 1. Schematics of one redox-level (red) energy diagram under application of different bias voltages. (a) Application of low bias voltage: the redox level lies below the Fermi window (yellow). (b) The same source-drain voltage under application of a gate voltage such that the redox level is available for conduction. (c) Conduction of the redox state using two-terminal configuration under application of high VSD.

appropriate gate voltage (VG) one can tune the molecular orbitals available for conduction within the Fermi window as determined by the source-drain voltage (VSD, see Figure 1). Here we show that the use of the MT allows scanning between a large variety of available potential combinations and thus includes many of the results obtained by other MJ tools. Moreover, we claim that the use of MT can predict ET results that might be obtained by future MJ experiments. This unique property of MT is exploited to investigate the puzzling issue of negative differential resistance (NDR) in redoxbased proteins. Received: March 6, 2011 Accepted: April 19, 2011 Published: April 25, 2011 1125

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Table 1. Reported Experimental Transport Data of Az in the Solid-State Configuration symmetry experimental

voltage

NDR (no. of peaks,

of the

system

range

voltage locations)

I/V curve

ref

yes

17

two-terminal planar transistor C-AFM

3 to 3

2: 2.2, 2.8

0 to 6 1 to 1

0 0 (at low and

not measured 18 yes

16

yes

16

high forces) C-AFM

4 to 4

2:

2, 3 at

intermediate forces

Figure 2. Top: Structure of Az (left) and apo-Az proteins (right). Bottom: Schematic presentation of the vertical MT, which is comprised of Si (1), SiO2(2), Si3N4 (3), Au source electrode (S,4), Pd drain electrode (D,5), Ti and its oxide gate electrode (G, 6,7, respectively) and the protein SAMs (8).

We recently introduced a solid-state MT that allows the investigation of MJ via transistor configuration.7 9 The device is termed a “Central-Gate Molecular Vertical Transistor” (C-Gate MolVeT, Figure 2 bottom) comprising a central or side Ti/TiO2 gate electrode that is used to activate a self-assembled monolayer (SAM) sandwiched between source and drain metal leads. We have shown that this transistor successfully “lights up” the molecular energy levels, even at low gate voltages. Here we utilize the MT to investigate the redox-based protein azurin (Az) and its nonredox derivative (apo-Az, see Figure 2). This type of protein has been extensively studied with the use of various techniques (Table 1), and thus the results can be compared to our transistor measurements. Az belongs to a special class of biomolecules called redox metalloproteins, which play a crucial role in biological ET in living matter.10,11 As such, they take part in a wide range of biological tasks that include energy metabolism (photosynthesis, respiration, and nitrogen fixation), hormone biosynthesis, and xenobiotic detoxification. For ET investigation, Az serves as a good model system since it includes some cysteine moieties, which facilitate SAM formation via the establishment of chemical bonds between the protein thiol groups and metallic surfaces, while its β-barrel conformation endows the protein with excellent mechanical resistance (see ref 20 and Supporting Information for SAM characterization details).12 Furthermore, the comparison between the ET results of Az and apo-Az with the use of the transistor allows us to determine whether the protein’s redox center is directly correlated to the key phenomena of NDR.4,13 Generally, the NDR signature appears as a distinct peak in the I/V curve and it is believed to originate

two-terminal

1 to 1

0

no

19

two-terminal

0.5 to 0.5

0

yes

20

from several possible mechanisms, such as polaron formation, resonance tunneling, and conformational changes of the measured molecule.4,5 It is usually found in molecules that carry redox centers (such as Az), although direct correlation between NDR and the redox center has not been experimentally verified. The results of previous transport-data experiments performed on Az are summarized in Table 1. It can be seen that a large variety of results has been obtained. Davis et al., using conducting atomic force microscopy (C-AFM),14 16 showed that the I/V behavior of an Az layer is force-dependent: it was found that NDR appeared only under the application of intermediate forces. In this particular regime, it was claimed that two-step tunneling through the redox state of the Az took place around applied voltages of 3 V. This finding is in agreement with the work of Maruccio et al., who found, with the use of a sophisticated two-terminal junction, two NDR peaks at ∼ ( 3 V.17 Surprisingly, no NDR peaks were obtained by the same group utilizing three-terminal configuration, even at 6 V.18 Although considerable variation is found in the appearance of NDR over the high-voltage range, it is commonly agreed that no NDR occurs on application of bias voltages of less than 1 V. To date, only one Az-based transistor has been demonstrated.18,21,22 However, in this lateral-type transistor, the charge flow between the source and the drain was perpendicular to the axis of a packed Az monolayer and not through its main axis. As expected, it was found that high voltages were needed to obtain low currents without the formation of NDR, even under application of high source-drain (VSD) and gate (VG) voltages (VSD, VG > 3 V).18 It should also be noted that, while in some experiments symmetrical source-drain contacts were used, such as Au Az Au MJ,17,20 in others, asymmetrical junctions (e.g., Si Az Au) were investigated.19 It had been previously been pointed out that the results obtained using nonidentical contact leads were definitely manifested in the I/V characteristics such as rectification, charging, and even NDR formation.4,5,23,24 Two types of devices were fabricated and measured with the use of a previously published procedure.7 The first device included a well-folded copper-free apo-Az monolayer, and the second transistor was composed of a standard Az SAM. Figure 3 shows room-temperature transistor transport data (ISD/VSD) obtained for the two transistor devices at various values of VG. Each device has been measured for 10 cycles. NDR reproducibility has been obtained, indicating the stability of the device and the lack of filament formation. This particular voltage regime has been chosen since we found that at higher gate 1126

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Figure 3. Room-temperature transistor transport data taken for the apo-Az (a) and the Az (b) devices. Clear NDR peaks (horizontal black arrows) are measured only at the Az device. VG was scanned from 0.4 to 0.4 V (increments of 0.1 V) for the two devices.

voltages one could not ignore the leakage currents or the formation of filaments.9,13 It can be seen that the current values obtained for the transistors are of similar magnitude, indicating that the ET originates from a similar number of molecules in both devices. Our results resemble the observations of Davis et al.,15 who did not find any significant current differences between an Az and a nonredox protein using scanning tunneling microscopy (STM) at the low I/V regime. These findings are in contrast to previous observations,18,19 where a large variation of the conductance-magnitude between the Az and its apo-form were obtained. Thus, we assume that our experimental system is somehow closer to the STM configuration since we measure small amounts of standing proteins with large gate sensitivity. This is in contrast to other works,18,19 which measured either the conductance perpendicular to the monolayer main axis or through large-area SAMs. In the latter cases, it is assumed that the effect of interproteins influences the conductance.25,26 In addition, we found that the two transistors showed ambipolar properties, as we have previously indicated.7 For both devices, a large response to VG at negative VSD was recorded, while the measured gate-leakage current was negligible. From a certain value of VG, the two spectra differ significantly. While in the apo-Az device a smooth monotonic I/V response was observed, even at high gate voltages, clear NDR peaks were measured at high gate voltages for the Az transistor even at VSD < 1 V. This important observation clearly indicates a direct and straightforward correlation between the redox center in Az and the NDR phenomenon in the solid phase. Furthermore, the unprecedented low-voltage NDR peak observed implies the ability of VG to tune the molecular energy levels (Figure 1). It can therefore be expected that this peak may be obtained in future experiments with other MJs. In order to compare our measurements with the other reported results, we measured the transconductance of the device as well as carrying out a high-voltage two-terminal experiment in which the gate electrode was disconnected. Figure 4a shows a clear NDR peak obtained at 3 V (compared to 0.6 V obtained with the use of a gated device), in excellent agreement with previous two-terminal observations.17 Additional representative

Figure 4. Az devices characteristics taken at different operation conditions which demonstrate the devices ability to reconstruct I/V received for various types of devices. (a) Two-terminal measurement exhibiting NDR at high voltage. (b) Symmetrical transistor I/V characteristics taken at low source-drain voltages with VG = 0.15. (c) Asymmetrical transistor characteristics obtained at VG = 0. (d) Transconductance measurements of the Az transistor taken for two VSD values.

ET curves, obtained at the “non-NDR regime”, utilizing various combinations of VSD and VG, are shown in Figure 4b,c. Notably, in this regime the symmetry of the curves could be easily varied. Figure 4d shows transconductance data taken at two different values of VSD. An apparent peak in the data was obtained over a certain range of VG, in agreement with the other transconductance data obtained for the lateral Az transistor. The excellent agreement with previously obtained data for two- and three-terminal devices proves that the use of vertical 1127

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The Journal of Physical Chemistry Letters transistors for conduction measurements can give a complete and comprehensive description of the various ET effects measured for various experimental systems In conclusion, we have shown that the use of vertical transistors for conduction measurements can provide a comprehensive description of the various ET effects as measured for various experimental systems. With the use of this technique, we have indicated the direct correlation between the existence of redox centers in molecules and the appearance of an NDR peak. Furthermore, this configuration may reveal low-voltage NDR peaks in other systems for which they have not, as yet, been observed. Reproduction of I/V data acquired by various techniques with the use of the transistor has been successfully demonstrated.

’ ASSOCIATED CONTENT

bS

Supporting Information. Apo-Az preparation, SAMs preparation and characterization, and device measurement setup. This material is available free of charge via the Internet at http:// pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected].

’ ACKNOWLEDGMENT The authors thank Mrs. Netta Hendler and Mr. Noam Sidelman for technical support, and Dr. Michael Gozin for protein supply. This work was partly supported by the Clal Biotechnology Fund, USAF (Project No. 073003), and the James Frank Foundation. ’ REFERENCES (1) Akkerman, H. B.; de Boer, B. Electrical Conduction through Single Molecules and Self-Assembled Monolayers. J. Phys.: Condens. Matter 2008, 20, 013001. (2) Mentovich, E. D.; Kalifa, I.; Tsukernik, A.; Caster, A.; RosenbergShraga, N.; Marom, H.; Gozin, M.; Richter, S. Multipeak NegativeDifferential-Resistance Molecular Device. Small 2008, 4, 55–58. (3) Blum, A. S.; Kushmerick, J. G.; Long, D. P.; Patterson, C. H.; Yang, J. C.; Henderson, J. C.; Yao, Y. X.; Tour, J. M.; Shashidhar, R.; Ratna, B. R. Molecularly Inherent Voltage-Controlled Conductance Switching. Nat. Mater. 2005, 4, 167–172. (4) Galperin, M.; Ratner, M. A.; Nitzan, A. Hysteresis, Switching, and Negative Differential Resistance in Molecular Junctions: A Polaron Model. Nano Lett. 2005, 5, 125–130. (5) Yeganeh, S.; Galperin, M.; Ratner, M. A. Switching in Molecular Transport Junctions: Polarization Response. J. Am. Chem. Soc. 2007, 129, 13313–13320. (6) Song, H.; Kim, Y.; Jang, Y. H.; Jeong, H.; Reed, M. A.; Lee, T. Observation of Molecular Orbital Gating. Nature 2009, 462, 1039–1043. (7) Mentovich, E. D.; Belgorodsky, B.; Kalifa, I.; Cohen, H.; Richter, S. Large-Scale Fabrication of 4-nm-Channel Vertical Protein-Based Ambipolar Transistors. Nano Lett. 2009, 9, 1296–1300. (8) Mentovich, E. D.; Belgorodsky, B.; Kalifa, I.; Richter, S. 1-Nanometer-Sized Active-Channel Molecular Quantum-Dot Transistor. Adv. Mater. 2010, 22, 2182–2186. (9) Mentovich, E. D.; Richter, S. The Role of Leakage Currents and the Gate Oxide Width in Molecular Transistors. Jpn. J. Appl. Phys. 2010, 49, 01AB04. (10) Farver, O.; Zhang, J. D.; Chi, Q. J.; Pecht, I.; Ulstrup, J. Deuterium Isotope Effect on the Intramolecular Electron Transfer in Pseudomonas aeruginosa Azurin. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 4426–4430.

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