S-Layer Protein for Resistive Switching and Flexible Nonvolatile

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S-layer protein for Resistive Switching and Flexible Nonvolatile Memory Device Akshay Moudgil, Neeti Kalyani, Gaurav Sinsinbar, Samaresh Das, and Prashant Mishra ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.7b15062 • Publication Date (Web): 08 Jan 2018 Downloaded from http://pubs.acs.org on January 8, 2018

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ACS Applied Materials & Interfaces

S-Layer Protein for Resistive Switching and Flexible Nonvolatile Memory Device Akshay Moudgil,1§ Neeti Kalyani,2§ Gaurav Sinsinbar,2 Samaresh Das,1 and Prashant Mishra2* 1

Centre for Applied Research in Electronics, Indian Institute of Technology Delhi, Hauz Khas,

New Delhi 110016, India 2

Department of Biochemical Engineering and Biotechnology, Indian Institute of Technology

Delhi, Hauz Khas, New Delhi 110016, India *Corresponding author. Tel: (+91) 01126591015; E-mail: [email protected] KEYWORDS: resistive switching, non-volatile memory, flexible electronics, bionanodevices, S-layer protein

ABSTRACT: In this work, flexible resistive switching memory device consisting of S-layer protein is demonstrated for the first time. This novel device (Al/Slp/ITO/PET) based on simple and easy fabrication method is capable of bistable switching to low resistive state (LRS) and high resistive state (HRS). This device exhibits bistable memory behavior with stability and long retention time (>4x103 s), stable up to 500 cycle endurance test and significant HRS/LRS ratio. The device possesses consistent switching performance for more than 100 times bending, corresponding to desired applicability for biocompatible wearable electronics. The memory mechanism is attributed to trapping/de-trapping process in S-layer protein. These promising

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results of the flexible memory device could find a way in the wearable storage applications like smart bands and sports equipment’s sensors.

1. INTRODUCTION The extensive advancement in the digital electronic systems has triggered an urgent need for miniaturization of these systems and developing materials with superior performance. Therefore, new materials have been sought after as an alternative to silicon-based devices to overcome their limitations.1,2 Inspired by nature, several biomolecules are potential candidates for electronic devices due to their inherent properties like biocompatibility, light weight, simple fabrication process and ease to transfer on flexible substrates. These systems involve discrete processes like the generation, transfer, storing and processing of information through electronic signals via various reactions.3 Biomolecules with desired functions, structures and self-assembly characteristics have an added advantage in miniaturization, and biodegradability.4 Moreover, biological processes are dynamic, efficient and precise, and hence can be used as biomimetic alternatives in the field of molecular electronics.5,6 Previous research with biomolecules like proteins have already been reported for the development of transistors,7 memory devices,8 biosensors,9 and light emitting diodes.10 Resistive switching devices based on azurin,11 silk fibroin,12 egg albumin,13 ferritin,14 and bacteriorhodopsin15 have also been studied. S-layer protein (Slp) has been employed in this study, which is present as an outermost layer of the cell envelope of walled bacteria and archaea.16–18 The Slps have been found in some species of Lactobacillus such as L. acidophilus, L. gallinarum, L. casei, L. buchneri, L. bulgaricus, L. kefir and L. brevis.19,20 These proteins are attached to the cell envelope by noncovalent bonds in a highly organized manner forming various patterns.18 Their molecular weight


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varies between 40-200 kDa and consists of similar monomeric proteins or glycoprotein sub-units which are able to self-assemble themselves into a pattern and hence forming isoporous patterned monolayers.21 Slps form highly porous and approximately 10 nm thick protein mesh, which have different lattice arrangements like square, hexagonal and oblique symmetry22 with unit size ranging between 3-30 nm. The arrangements depend on the source microorganism of Slp.23 Slp is particularly suited and favorable candidate for the patterning applications in bionanotechnology and bio-mimetics because of its inherent potential to recrystallize in a specific array in suspension, on solid surfaces and on a diverse lipid structures.24,25 Slp has been used as building units for the precise bottom-up fabrication of different interfaces and molecular conformations. Previous research have shown application of some biomolecules like proteins, nucleic acids, lipids, glycans in various devices,26 but application of Slp in the non-volatile memory devices have not been reported yet. In this work, the behavior of S-layer protein for the development of a novel resistive memory device on flexible substrate have been examined. For this, the S-layer protein was cloned, overexpressed and purified in large amount. The protein was immobilized on flexible ITO substrates, and its memory characteristics were studied. 2. MATERIALS AND METHODS S-layer gene from Lactobacillus brevis ATCC 8287 was cloned in fusion with 6 x histidine tag in Escherichia coli. Thereafter S-layer protein was over expressed and purified using Ni-NTA chromatography.


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For the immobilization of S-layer protein, the ITO substrates were functionalized with MPTS (3mercaptopropyltrimethoxysilane). The S-layer protein (10 mg/ml) was immobilized by incubating the substrates with protein overnight at 4˚C. The device was fabricated using ITO/PET (indium tin oxide/polyethylene terephthalte) flexible substrate where Slp film was deposited on ITO. Then, Slp was etched off from the half portion of the flexible device and this portion act as ground terminal for electrical characterization. Aluminum electrode having diameter 1mm was patterned by shadow mask to act as the top electrode and ITO act as a bottom electrode on Slp/ITO/PET cell structure. 3. RESULTS AND DISCUSSION Slp was chosen for this study because of the following reasons: i) Slp is hydrophilic (GRAVY index = -0.406) and stable (instability index = 0.88) as determined by ProtParam (http://web.expasy.org/cgi-bin/protparam), ii) Slp is redox inactive and hence can be used for memory applications (Figure S1), iii) Slp is majorly composed of β-sheets (Figure 1) similar to sericin protein, which has shown excellent memory behavior,27 iv) Slp layer thickness can be monitored with incubation time (Figure 2).The light scattering intensity from the self-assembled complex arrangement of Slp depends on both: the number of Slp molecules forming the complex and the size of complex formed.28 We used the dynamic light scattering (DLS) data to optimize the CaCl2 and protein concentration required for the self-assembly of Slp. After 9 hours the size distribution of Slp protein crystalline domains in solution was large, but with time the size distribution narrows down to small range. A schematic illustration (Figure 2) of the process of self-assembly of S-layer proteins in solution was deduced on the basics of the data obtained from DLS.28,29


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The simple Al-protein-ITO/PET (indium tin oxide/polyethylene terephthalte) device structure which is shown in Figure 3a, was used to examine the non-volatile memory characteristics in Slp. Figure 3b shows the typical atomic force microscopy (AFM) image of Slp immobilized on ITO/PET where roughness around 6.3 nm was observed. Figure 3c shows the cross-sectional scanning electron microscopy (SEM) image of device, where distinctive layer by layer configuration was confirmed. Optical image shown in Figure 3d corresponds to bending capability of the device. Figure 4a illustrates typical I-V characterization of the Al/Slp/ITO/PET device under sweeping mode where the Al/Slp/ITO electrode act as top terminal and Al/ITO electrode as ground terminal. When the voltage sweep from 0 V to set voltage (Vset), the device switched from high resistive state (HRS) to low resistive state (LRS). In the next sweep from 8 V to 0 V, the memory device stays in the low resistive state. During the sweep from 0 V to -8V, low resistive state switch back to high resistive state of the device. The

I-V characteristics

repeatability was also investigated for more than 500 cycles which are comparable to reported earlier.30 Figure 4b shows the I-V characteristics for ten cycles with a higher degree of consistency. The endurance parameters were extracted at a read voltage of 5 V. Figure 4c shows the assessment of memory performance of the novel Slp based flexible device at room temperature. The retention characteristics was measured under 5 V read voltage. The device exhibited very stable LRS and HRS states over the 500 cycle measurements with less than ±5% variation, as shown in Figure 4d. This Slp based device exhibit bipolar memory as it sustain only two states for positive as well as negative sweeps. The resistance of both states was almost constant for more than 4x103 s and did not show resistance variation for more than ±0.3 kΩ. A significant LRS to HRS switching ratio around 6.2 was obtained in the Slp memory device.


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However, the device can be operated in lower read voltage with two repeatable stable states as shown in Figure 4 (b). For example, the device shows 4.05 and 5.9 LRS to HRS ratio at 2 V and 4 V read voltage, respectively. The major advantage for any flexible device is their bending capability up to an extent which does not affect the device performance. So, to examine such important aspect, the device was bent more than 100 times at radius of curvature (ROC) = 28.5 mm. Figure 4e shows the steady bending characteristics with very consistent switching states at 5 V read voltage. As the bending number goes up, there was slight decrement in the LRS and HRS. To further investigate the bending performance, flexible device was bent for various bending radius of curvature. Figure 4f demonstrate the LRS/HRS variation with radius of curvature (Flat to 9.5 mm). The variation in the LRS and HRS could be observed for different radius of curvature. Due to the higher bending stress, maximum variation is observed for 9.5 mm radius of curvature. The prominent results obtained in this study suggest that the Slp based novel memory device can be conceivable for non-volatile memory applications. The resistive switching mechanism in memory devices occurs due to three proposed phenomenon as 1) redox reaction of materials 2) metal filament formation and 3) trapping/detrapping process within the switching materials.27,31 To probe the switching mechanism of the Slp device for redox reaction properties, electrochemical analysis was carried out using cyclic voltammetry. However, no oxidation/reduction peaks were observed in the cyclic voltammogram (Figure S1). Secondly, the conception that facile oxidation is accountable for electrochemical memory effect in Al/Slp/ITO configuration is ruled out by assessing the device. The aluminium electrodes symmetry also possesses resistive switching memory behavior. The Slp act as a semiconductor/ insulator inherently (observed from cyclic voltammogram) and absence of permanent memory without applied voltage, rule out the possibility of metal filament


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formation.32 Therefore, the trapping/de-trapping process in Slp layer could be attributed to the resistive switching mechanism. The output characteristics is confined by the space charge limited current (SCLC) model.32 The I-V characteristics in log-log scale could be partitioned into two regions as shown in Figure 4 (a) inset. First, where the current is in linear scale and second after nonlinearity in the current curve, which signify the ohmic and trap free space charge limit current, respectively. An equation model of the trap affected current in the slp layer can be given by following equations31, where the transport current is J, free charge concentration is n, free carrier concentration of the trapped charge is nt, dielectric constant of the material is ε, free carrier mobility is µ, applied voltage is V, and layer thickness is L.

J =

9 n µε V 2 8 n t L3

(with traps) (1)

J =

9 µε V 2 8 L3

(filled traps)

(2)

Initially, with small applied voltage, the number of the injected carrier is smaller than thermally injected carrier due to very small electric field application. In the nonlinear region, more charge carriers were injected from the electrode due to increase in applied voltage. The excess charge carrier generation could not be accommodated by the bulk material, and accordingly, space charges are formed in vicinity of the interface of electrode, leading to the SCLC conduction mechanism.32 The LRS mechanism in Slp memory device may correspond to


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the hopping conduction as available trap centres are already filled by the injected carries. In HRS, Slp film shows near to non-conductiong property as there may be few defects prompted at the Slp and aluminium electrode interface.27 When the voltage is applied, first empty sites will be filled by charge carriers injected from the electrode which follows equation (1). Hence free

J =

− 4 2 m * (qφ )3 / 2 E 2 q2E 2 exp[ ] 2 16 π φ h 3 h qE

charge concentration ‘n’ will starts to increase. Then, as the

voltage increased, at a certain voltage, free charge will be accommodated by trap sites and get filled. These filled sites with charge carriers as described by (2) will form a conductive path and this mechanism is illustrated in Figure 5 for Slp film. For the higher bias, transport mechanism can be quantified by Fowler-Nordeim tunneling expression given by equation33 (3), where E is electric field, charge is q, electron mass is m*, (3)

energy barrier is Փ , reduced Planck constant is ℏ . For the tunneling process, ln(J/V2) vs 1/V (V1

) is plotted where linearity in the curve for more than 6 V (0.125 V-1 – 0.166 V-1) applied

voltage is observed as shown in Figure 6. At higher bias, current shoots up due to F-N tunneling as shown in Figure 6 inset. Environmental stability test was performed for the long term performance of the Slp based flexible memory device. The device was tested under ambient condition for a consecutive span of 4 weeks. Figure 7a shows the stability of both resistive states where no obvious change was observed for the entire test span. The longevity feature of this device emulates its feasibility


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to employ in various biocompatible applications. Device to device set voltage and reset voltage distribution was studied as shown in Figure 7b.Ten devices were tested at ambient conditions for set and reset voltage consistency where an average swing of distribution was found to be ±0.15 V. This minimal swing entitles the device performance optimal for the memory operation. Device to device resistance of both resistive states at 5 V read voltage was investigated. Remarkably, highly stable and consistent HRS and LRS were obtained as shown in Figure 7c. Overall, for flexible memory applications, this device shows effective usability with high stability. The performance of the memory device can be improved in terms of on-off current ratio by changing active materials switching properties.

4. CONCLUSION Non-volatile resistive switching characteristics of the Slp flexible device has been demonstrated for the first time. This device exhibits bistable memory behavior with stability and long retention time (> 4x103 s), stable up to 500 cycle endurance test and significant HRS/LRS ratio. The device possesses consistent switching performance for more than 100 times bending, corresponding to desired applicability for biocompatible wearable electronics. Device to device distribution of Vset, Vreset and HRS, LRS turn out to be ±0.15 V and ±0.1kΩ, respectively. Remarkable environment stability was observed over a span of 4 weeks with no obvious fluctuations in both resistive states. The trapping/de-trapping of charge carriers and conduction via trapped charge carriers path seems to be responsible for the conduction mechanism of Slp based memory device. This non-volatile memory can be used for active memory storage in a


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powered off state of electronic chips. These low cost biocompatible flexible Slp based memory devices could find a way in the wearable storage applications like smart band etc.


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Figure 1. (a) Secondary structure of Lactobacillus brevis Slp predicted by PSIPRED online server (http://bioinf.cs.ucl.ac.uk/psipred), and (b) 3-dimensional structure of Slp predicted by Phyre2 web server (http://www.sbg.bio.ic.ac.uk/phyre2).


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Figure 2. Schematic representation of single crystal growth of S-layer protein and preceded by the amorphous to crystal transaction of the S-layer proteins. 1. Lyophilised S-layer proteins have random aggregates of various sizes distribution as observed using dynamic light scattering. It is schematically represented in intensity vs. size (nm) graph obtained by dynamic light scattering. 2. Aggregated or amorphous sate of S-layer proteins. 3. The amorphous state restructures to initiate nucleation of S-layer protein to form ordered self-assembled monolayers in solution. 4. The nucleation sites grow in large self-assembled mono layers and the growth takes place by the assembly of monomeric S-layer proteins at the kink sites (red colour). The size distribution also narrows down as amorphous to crystal transaction of the s-layer proteins take place. 5. The selfassembled monolayers of S-layer proteins attain an equilibrium and after a certain size the sheets starts precipitating because of large size. The sheets size narrow down as observed using DLS.


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Figure 3. (a) Schematic of fabricated flexible memory device with symmetric electrode configuration.

(b) AFM image of Slp, having 6.3 nm roughness. (c) Scanning electron

microscopy image of the cross-section of device structure. (d) Optical image of Slp memory device on flexible substrate.


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Figure 4. (a) Current vs. voltage (I-V) curves of the Al/Slp/ITO device in voltage sweep mode at ambient condition (log(Current)-log(V) plot in the inset) (b) Repeatability test for current vs. voltage (I-V) characteristics, (c) Retention characteristics under 5V read voltage. (d) Endurance characteristics under 5V read voltage. (e) Bending characteristics of flexible device for both resistive state at 5V read voltage. (f) The variation of HRS/LRS with bending radius of curvature (flat to 9.5 mm).


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Figure 5. Schematic diagram for the conduction mechanism in Slp based memory where the hollow circle in Slp represent unfilled charge site while the filled circle portray filled charge site.(a) Initial high resistance state without external bias. (b) Applied voltage inject charge from electrode to fill few empty charge site. (c) After applying set voltage, most of the empty site is filled with charge and hopping of charge from one filled site to other initiated which correspond to low resistance state.(d) Applied reset voltage correspond to breakage of conductive path and few sites left fully filled and the device switches to HRS.


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Figure 6. ln(J/V2) vs 1/V (V-1) curve for the LRS, inset shows ln(J/V2) vs 1/V (V-1) FowlerNordeim tunnelling at higher bias.


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Figure 7. (a) Stability test of both resistive states over the 4 weeks span of the Slp based flexible memory device (b) Device to device distribution of Vset and Vreset, where the results are extracted data from 10 devices. (c) Device to device distribution of resistance of both resistive states at 5V read voltage for 10 devices.


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ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Cyclic voltammogram of Slp AUTHOR INFORMATIONS Corresponding author *

E-mail: [email protected]

Author’s Contribution The manuscript was written through the contributions of all authors. All authors have given approval to the final version of the manuscript. §These authors contributed equally. Notes The authors declare no competing financial interest. ACKNOWLEDGMENTS The work was partially supported by the Ministry of Electronics and Information Technology (MeitY), Government of India. Akshay Moudgil received financial support from Ministry of Electronics and Information Technology, New Delhi. Neeti Kalyani acknowledges financial support from Council of Scientific and Industrial Research, New Delhi. ABBREVIATIONS Slp, S-layer protein;

ITO, indium tin oxide; PET, polyethylene terephthalate; MPTS, 3-

mercaptopropyltrimethoxysilane; LRS, low resistive state; HRS, high resistive state


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Graphical Abstract


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S-Layer Protein for Resistive Switching and Flexible Nonvolatile

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