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Virus-Enabled Synthesis and Assembly of Nanowires for Lithium Ion Battery Electrodes

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Science  12 May 2006:
Vol. 312, Issue 5775, pp. 885-888
DOI: 10.1126/science.1122716

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Abstract

The selection and assembly of materials are central issues in the development of smaller, more flexible batteries. Cobalt oxide has shown excellent electrochemical cycling properties and is thus under consideration as an electrode for advanced lithium batteries. We used viruses to synthesize and assemble nanowires of cobalt oxide at room temperature. By incorporating gold-binding peptides into the filament coat, we formed hybrid gold–cobalt oxide wires that improved battery capacity. Combining virus-templated synthesis at the peptide level and methods for controlling two-dimensional assembly of viruses on polyelectrolyte multilayers provides a systematic platform for integrating these nanomaterials to form thin, flexible lithium ion batteries.

There is an increasing need for smaller and more flexible Li ion batteries and for methods to assemble battery materials. Nanoparticles, nanotubes (1, 2), and nanowires (3), as well as several assembly methods based on lithography, block copolymer (4), or layer-by-layer deposition (5), have been introduced for constructing dimensionally small batteries. In addition to their utility in nanoelectronics, there is also growing evidence that nanostructured materials can improve the electrochemical properties of Li ion batteries compared to their bulk counterparts (6). However, to maximize this potential, monodisperse, homogeneous nanomaterials and hierarchical organization control are needed. Biosystems have the inherent capabilities of molecular recognition and self-assembly and thus are an attractive template for constructing and organizing the nanostructure (713). We have previously used viruses to assemble semiconductor and magnetic nanowires (14, 15) and consider whether they can be used for device fabrication. Using batteries as our example device, we also explore whether the viruses can be modified to improve the electrode materials. Because the viruses can assemble on multiple length scales, there may be scope for designing hierarchical self-assembling batteries. For this biological approach, once the genes are programmed for a functional device, very little postsynthesis processing is necessary. Additionally, this biological route uses room-temperature, aqueous synthesis conditions.

The M13 virus consists of ∼2700 major coat proteins (p8) helically wrapped around its single-stranded DNA, with minor coat proteins (p3, p6, p7, and p9) at each end of the virus. The functionality of these subunit proteins can be modified specifically through additions in the M13 genome. Modification of the major coat proteins, as well as minor coat proteins at the virus ends, has been used successfully to form functional heterostructured templates for precisely positioned nanomaterials (16, 17). Furthermore, the intrinsically anisotropic virus structures are well suited for the growth of monodisperse, highly crystalline nanowires (14, 15). In addition, the anisotropic virus structures are promising as elements of well-ordered nanostructure, as demonstrated in three-dimensional (3D) liquid crystal film (18, 19).

Predictive-based design was used for engineering the virus to satisfy the multifunctional purpose of electrode formation and assembly with a polymer electrolyte for the Li ion battery (Fig. 1). Tetraglutamate (EEEE-) was fused to the N terminus of each copy of the major coat p8 protein with 100% expression. This clone, named E4, was designed with three objectives. (i) It can serve as a general template for growing nanowires through the interaction of the glutamate with various metal ions (Virus Bio-templating in Fig. 1). Carboxylic acid, the side chain of glutamate, binds positive metal ions via ion exchange, as demonstrated in polymeric templates (20). Glutamateisalsobelievedtobe important in biomineralization, as evident in its role in specific proteins that regulate the nucleation of biominerals in nature. (ii) Tetraglutamate acts as a blocking motif for gold nanoparticles (21), due to the electrostatic repulsion. Therefore, tetraglutamate reduces nonspecific gold nanoparticle binding to phage, thereby increasing the specificity of a gold-specific peptide to bind gold in low concentration. (iii) The E4 clone is ideally suited for electrostatically driven assembly with a charged polymer (Assembly Engineering in Fig. 1). E4 is more negatively charged than wild-type virus, which enables it to interact favorably with the positively charged electrolyte polymer. Zeta potential measurements of the E4 clone reveal a dramatic change in the potential between pH 4.5 and 5.5, thus enabling a certain degree of charge control.

Fig. 1.

Schematic diagram of the virus-enabled synthesis and assembly of nanowires as negative electrode materials for Li ion batteries. Rationally designed peptide and/or materials-specific peptides identified by biopanning were expressed on the major coat p8 proteins of M13 viruses to grow Co3O4 and Au-Co3O4 nanowires. Macroscopic ordering of the engineered viruses was used to fabricate an assembled monolayer of Co3O4 nanowires for flexible, lightweight Li ion batteries.

To design the cobalt oxide (Co3O4) nanowires electrodes, we incubated the E4 virus templates in aqueous cobalt chloride solution (1 mM) for 30 min at room temperature to promote cobalt ion binding (22). Co3O4 was chosen as one of a family of new lithium-active compounds with an extremely large reversible storage capacity arising from displacement reactions (23), approximately three times as large as the capacity of carbon-based anodes currently used in commercial batteries. After reduction with NaBH4 and spontaneous oxidation in water, monodisperse, crystalline Co3O4 nanowires were produced (24). Figure 2, A and B, shows transmission electron microscope (TEM) images of the virus-templated Co3O4 nanowires, where Co3O4 nanocrystals of ∼2 to 3nm in diameter were uniformly mineralized along the length of the virus. For TEM observation, a dilute suspension was dropped on a carboncoated TEM grid, washed with distilled water, and dried. The high-resolution TEM electron diffraction pattern and lattice spacing (Fig. 2), together with x-ray diffraction, confirm that the crystal structure is Co3O4. The inset in Fig. 2B shows that the measured lattice spacing corresponds to the planes of Co3O4. Because p8 proteins were genetically engineered with 100% expression and cobalt ions have a strong binding affinity to the carboxyl groups of glutamate, homogeneous and high-crystalline nanowires were synthesized. Furthermore, viral Co3O4 nanowires had a large surface area of 141.7 m2/g, as measured by the Brunauer-Emmett-Teller method. The mass ratio of Co3O4 and virus is 0.837:0.163. Unlike E4 viruses, Co3O4 nucleating viruses, solutions of wild-type virus expressing no peptide insert, or solutions without viruses formed irregular and large precipitates of Co/Co3O4 mixtures.

Fig. 2.

Characterization of the Co3O4 nanowires templated by M13 virus. (A) TEM image of virus-templated Co3O4 nanowires. For visualizing the individual wires, the nanowires solution was diluted 1:100. (B) High-resolution TEM image of a Co3O4 viral nanowire. Electron diffraction pattern (Inset, upper right) confirmed that the crystal structure was Co3O4. Magnified image (inset, lower right) shows the lattice fringe of Co3O4 nanocrystals along the major coat p8 proteins of a virus. The measured lattice spacing corresponds to the (311) and (400) planes of Co3O4.(C) Charging-discharging curves for a virus-mediated Co3O4/Li half cell cycled between 3 and 0.01 V at a rate of C/26.5. C was defined as eight Li ions per hour. (D) Specific capacity versus cycle number for the same cell. The mass of Co3O4 only was considered. For comparison, data for the powder that was fabricated without viruses under the same condition are shown. (E) TEM images of differently nanostructured Co3O4 viral nanowires that were fabricated at a higher cobalt ion concentration. (F) TEM images of the assembly of discrete Co3O4 nanocrystals (on the p8 proteins), which were synthesized at 4°C.

For electrochemical evaluation of the Co3O4 nanowires, positive electrodes were prepared by mixing together 3.29 mg of the virus-based nanowires, Super P (MMM Carbon, Brussels, Belgium) carbon black, and poly(vinylidene fluoride)-hexafluoropropylene binder in a mass ratio of 74:15:11. Swagelok design cells using Li metal foil used as the negative electrode and a separator film of Celgard 2400 were assembled and saturated with the liquid electrolyte, 1MLiPF6, in ethylene carbonate and dimethyl carbonate (1:1 by volume). The assembled cells were galvanostatically cycled between 3.0 and 0.01 V using a Maccor automated tester. The behavior of voltage/capacity curves (Fig. 2C) for the Co3O4/Li half cell was similar to that of Co3O4 nanoparticles produced by other methods (25). The larger first-insertion capacity compared to that in subsequent discharge is characteristic of this material and is due to irreversible reactions occurring upon initial lithiation. Any biphasic nature (25) of Co3O4 and LixCo3O4 (∼Li1.47Co3O4) at the early stages of discharge was not clearly evident from the voltage traces (Fig. 2C). We observed reversible capacity (Fig. 2D) ranging from 600 to 750 mA·hour/g, which is about twice that of current carbon-based negative electrodes. The charge and discharge capacities stabilized at 600 mA·hour/g over 20 cycles. The reversible formation of Li2O accompanying the redox of cobalt nanoparticles and the reversible growth of a gel-like polymeric layer (26), resulting from electrolyte degradation, are believed to contribute to this reversible capacity. The existence of higher than theoretical specific capacity in Co3O4 has been observed before (27), and it plausibly attributed to the reversible formation of a Li-bearing solid-electrolyte interface. At the nanometer scale, both the reversible formation of Li2O, which is known to be electro-chemically inactive in bulk, and the reversible formation of the gel-like layer catalyzed by cobalt nanoparticles can occur (23). A control experiment revealed that the virus is electro-chemically inactive and stable over the electro-chemical conditions of our experiments, as indicated by the absence of decomposition in cyclic voltammograms (fig. S1). The virus capsid–mediated growth of uniform-sized Co3O4 nanomaterials, in addition to the structural integrity and dense packing (Fig. 2B) imparted by the virus, provides electrochemical advantages. For instance, when all other experimental conditions were held constant, the capacity of samples fabricated without the virus templates faded rapidly (Fig. 2D). This phenomenon, which is most likely attributable to incomplete oxidation of cobalt, inhomogeneous composition, and large particle size, has also been observed for Co3O4 prepared at low temperatures, in which high polarization is a contributing factor (25). However, the properties of Co3O4 nanowires, templated by M13 virus and oxidized spontaneously at room temperature, were comparable to those of particles fabricated at temperatures above 500°C.

An added advantage of this system is that the nanotexture of viral Co3O4 nanowires can be manipulated by controlling the interactions between the peptides and cobalt ions. Higher cobalt chloride concentration (5 mM) with 10 mM NaBH4 produced branchlike nanowire structures (Fig. 2E); in contrast, nucleation and growth of Co3O4 nanowires at 4°C with 1 mM cobalt ion and 5 mM NaBH4 resulted in the assembly of discrete nanoparticles (Fig. 2F).

To design new hybrid material electrodes with higher capacity, we engineered additional material-specific peptide motifs into the major coat p8 protein. This provides a general method for the systematic and controlled arrangement of two distinct nanomaterials, which can enhance the electrochemical properties through the cooperative contribution of each material. Increasingly, efforts to improve battery properties have focused on composite material design (28, 29). However, notable challenges, such as the achievement of uniform distributions of multiple phases, are encountered when components are combined at the nanoscale. Gold nanoparticles were chosen on the basis of their ability to provide high electronic conductivity where needed, the ability to maintain a thermo-dynamically stable interface with Co3O4, and the potential to catalyze electrochemical reactions at the nanoscale. We designed a bifunctional virus template that simultaneously expressed two different peptide motifs. To accomplish this, we isolated a gold-binding peptide motif (LKAHLPPSRLPS) by screening against a gold substrate with a phage display library (30), which contains random 12–amino acid peptide sequences. Then, we assembled bifunctional viruses constructed to express both Au-Co3O4-specific peptides with the virus coat. Phagemid constructs (15) were inserted into host bacterial cells encoding the gold-binding peptide motif (31). Thus, upon infection of the plasmid-incorporating host cells with the E4 virus, a small percentage of the resulting E4 p8 proteins also displayed the gold-specific peptide. Therefore, two types of p8 proteins were produced: intact p8 proteins of E4 viruses and engineered p8 proteins containing the gold-binding peptide motif, randomly packaged onto the virus progeny (Fig. 3A). This hybrid clone was named AuE4 virus. Incubation of the amplified AuE4 clones with a 5-nm gold colloid suspension (5 × 1013 particles/ml; Ted Pella) resulted in 1D arrays of Au nanoparticles bound to the gold-binding peptides distributed among p8 proteins (Fig. 3B). In contrast, wild-type viruses and the E4 virus, which do not have gold-binding motifs, did not bind gold nanoparticles along the length of the virus. After removal of excess unbound gold nanoparticles by centrifugation, Co3O4 was nucleated and grown via the tetraglutamate functionality, resulting in hybrid nano-structures of 5-nm Au nanoparticles spatially interspersed within the Co3O4 wires (Fig. 3C). The crystal structure of the Co3O4 was confirmed by electron diffraction. Inductively coupled plasma mass spectrometry (ICPMS) analysis indicated that Au nanoparticles were associated with Co3O4 in a mass ratio of 0.024:0.976.

Fig. 3.

Characterization of the hybrid nanostructure of Au nanoparticles incorporated into Co3O4 nanowires. (A) Visualization of the genetically engineered M13 bacteriophage viruses. P8 proteins containing a gold-binding motif (yellow) were doped by the phagemid method in E4 clones, which can grow Co3O4. (B) TEM images of the assembled gold nanoparticles on the virus. Control experiments showed that gold nanoparticles were bound by the gold-specific peptides. (C) TEM image of hybrid nanowires of Au nanoparticles/Co3O4.(D) Specific capacity of hybrid Au-Co3O4 nanowires. Half cell with Li electrode was cycled at a rate of C/26.5. Virus mass was subtracted and the mass of active materials such as Co3O4 and Au was counted. The capacity of virus-directing Co3O4 nanowires without Au nanoparticles was also compared. (E) Cyclic voltammograms of hybrid Au-Co3O4 and Co3O4 nanowires at a scanning rate of 0.3 mV/s.

We evaluated the electrochemical properties of the hybrid Au-Co3O4 nanowires by using galvanostatic cycling and cyclic voltammetry. The mass of Au-Co3O4 nanowires deposited on the Cu substrate for one electrochemical cell was 3.41 mg. The virus-mediated hybrid composite generated higher initial and reversible lithium storage capacity than the pure Co3O4 nanowires when tested at the same current rate (Fig. 3D). The higher lithium storage capacity may result from the formation of Au-Li intermetallic compound or the conductive or catalytic effects of Au nanoparticles on the reaction of Li with Co3O4. Au is known to be electrochemically active, which leads to the formation of LixAu alloys (32). However, based on the Au:Co3O4 ratio, the contribution of LixAu alloys to the lithium storage capacity is likely negligible. Cyclic voltammetry (Fig. 3E) shows no notable new redox peaks that could be associated with the lithiation of Au (4). Given the unique charging/discharging mechanism of Co3O4, wherein cobalt nanoparticles promote the reversible reaction of an organic layer that then contributes to the Li capacity, it is more likely that Au nanoparticles play a role in this displacement reaction. This role may be one of improving electronic conductivity to the Co3O4 nanoparticles, or it may be catalytic in nature. Indeed, decreased cell polarization was observed in the galvanostatic voltage-capacity curves, which could result from either of these mechanisms. Furthermore, incorporation of Au clearly increases the reaction rate upon reduction of Co3O4, as indicated by the enhanced reduction peak seen by cyclic voltammetry in Fig. 3E (measured on samples of similar mass at the same voltage sweep rate). Although the exact electrochemical mechanism is under investigation, our results show that a small amount of Au nanoparticles dispersed within Co3O4 to produce a hybrid material markedly improves electrochemical performance. The specific capacity of the hybrid is estimated to be at least 30% greater than that of our Co3O4 nanowires.

The principles of self-assembly and bio-templating can be further extended to control virus-virus interactions for organizing nano-structured electrodes over large length scales. Recently, we observed that negatively charged M13 viruses can form very ordered, 2D liquid crystalline layers on top of electrostatically cohesive films of linear poly(ethylene imine) (LPEI)/poly(acrylic acid) (PAA) (33). The ordering of engineered viruses is driven by competitive electrostatic interactions, the interdiffusion of the polyelectrolyte, and the anisotropic shape of M13 viruses. By using this technique to spontaneously order E4 viruses and subsequently grow Co3O4 on the virus coat proteins, we produced 2D organized ensembles of nanowires on a 10-cm length scale (Fig. 4, A and B). The spatial distance and ordering behavior between viral nanowires can be manipulated by controlling both surface charge and fluidic forces. Furthermore, the thickness of the multilayered polymer can be varied from 10 nm to several micrometers, independent of the substrate. This assembly process produces lightweight, flexible, and transparent active material/substrate multilayers, constructed as free-standing films by a simple dipping method (Fig. 4C). This process should be scalable using roll-to-roll processing. Moreover, the polymer electrolyte is believed to act as a solid electrolyte because of the relatively fast ionic conductivity of LPEI and PAA pairs (34, 35). Thus, the assembled layers compose a negative-electrode material grown upon a solid electrolyte or separator membrane. For electrochemical evaluation, 100 nm of Cu, which functions as a current collector, was deposited by E-beam evaporation on the assembled Co3O4 nanowires/polymer layer. This assembly was then tested in Swagelok cells with a Li foil negative electrode separated from the multilayer by a separator dipped in liquid electrolyte (36). Figure 4D shows the capacity for the assembled monolayer of Co3O4 nanowires/Li cell at two different charging rates. The cell was found to sustain and deliver 94% of its theoretical capacity at a rate of 1.12 C and 65% at a rate of 5.19 C, demonstrating the capability for a high cycling rate. We believe that the power of the cell can be further increased by alternating stacks of nanowire monolayers and polymer layers of LPEI and PAA or other polyions. In addition, the Au-Co3O4 hybrid nanowires should also increase the total capacity.

Fig. 4.

Two-dimensional assembly of Co3O4 nanowires driven by liquid crystalline ordering of the engineered M13 bacteriophage viruses. (A and B) Phase-mode atomic force microscope image of macroscopically ordered monolayer of Co3O4-coated viruses. The Z range is 30° (C) Digital camera image of a flexible and transparent free-standing film of (LPEI/PAA)100.5 on which Co3O4 viral nanowires are assembled into nanostructured monolayer with dimensions of 10 cm by 4 cm. (D) Capacity for the assembled monolayer of Co3O4 nanowires/Li cell at two different charging rates.

Our results demonstrate that basic biological principles can be applied to the rational design and assembly of nanoscale battery components, exhibiting improved performance in properties such as specific capacity and rate capability. The genetic control in the viral synthesis of monodisperse oxide nanowires and the nanoarchitecture of hybrid nanowires can be advanced through further modification of other proteins. Heterostructured nanowires, composed of anode and solid electrolyte, and bioenergy-transducing nanowires, coupled with biomolecules, are currently being investigated. Moreover, we anticipate that self-organized virus monolayers for the generation of anodic as well as cathodic materials on ionically conducting polyelectrolyte films may present potential architectures for interdigitated batteries (37). The ease of genetic modification allows for the growth and assembly of other functional nanomaterials for applications such as photovoltaic devices, high–surface area catalysts, and supercapacitors.

Supporting Online Material

www.sciencemag.org/cgi/content/full/1122716/DC1

Fig. S1

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