Science Fabricating Genetically Engineered High-Power Lithium-lon Batteries Using Multiple Virus Genes Yun jung lee et al NAAAS Science324,1051(2009) Do:10.1126/ scIence.1171541 This copy is for your personal, non-commercial use only If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here The following resources related to this article are available online at www.sciencemag.org(thisinformationiscurrentasofSeptember17,2014): Updated information and services, including high-resolution figures, can be found in the online version of this article at http://www.sciencemag.org/content/324/5930/1051.fullhtml Supporting Online Material can be found at http://www.sciencemag.org/content/suppl/2009/04/01/1171541.dc1.html This article cites 25 articles, 5 of which can be accessed free http://ww.sciencemag.org/content/324/5930/1051.full.html#ref-list-1 This article has been cited by 11 article(s)on the iSI Web of Science This article has been cited by 9 articles hosted by HighWire Press http://www.sciencemag.org/content/324/5930/1051.fullhtmlrelated This article appears in the following subject collections Materials Science http://www.sciencemag.org/cgi/collection/matsci Science(print ISSN 0036-8075: online ISSN 1095-9203)is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2009 by the American Association for the Advancement of Science; all rights reserved. The title Science is a egistered trademark of AAAs
DOI: 10.1126/science.1171541 Science 324, 1051 (2009); Yun Jung Lee et al. Using Multiple Virus Genes Fabricating Genetically Engineered High-Power Lithium-Ion Batteries This copy is for your personal, non-commercial use only. colleagues, clients, or customers by clicking here. If you wish to distribute this article to others, you can order high-quality copies for your following the guidelines here. Permission to republish or repurpose articles or portions of articles can be obtained by www.sciencemag.org (this information is current as of September 17, 2014 ): The following resources related to this article are available online at http://www.sciencemag.org/content/324/5930/1051.full.html version of this article at: Updated information and services, including high-resolution figures, can be found in the online http://www.sciencemag.org/content/suppl/2009/04/01/1171541.DC1.html Supporting Online Material can be found at: http://www.sciencemag.org/content/324/5930/1051.full.html#ref-list-1 This article cites 25 articles, 5 of which can be accessed free: This article has been cited by 11 article(s) on the ISI Web of Science http://www.sciencemag.org/content/324/5930/1051.full.html#related-urls This article has been cited by 9 articles hosted by HighWire Press; see: http://www.sciencemag.org/cgi/collection/mat_sci Materials Science This article appears in the following subject collections: registered trademark of AAAS. 2009 by the American Association for the Advancement of Science; all rights reserved. The title Science is a American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the on September 17, 2014 www.sciencemag.org Downloaded from
REPORTS ot in the 33-ns experiment. This value is much n the dispersion of silver clusters on the 17. W. Perrie, A. Rushton, M. Gill, P. Fox, W. ONeill igher than rates obtained in steady-state con- st(32) analytically active Ag* clusters Appl Sur. Sci. 248, 213(2005 ditions with a similar catalyst and temperature on acid sites on the alumina support. The 19. M Bonn et al, Phys. Rev. B 61, 1101(2000). range(29). The rate-determining step in the steady- bridged intermediate reported here can only be 20. C Voisin et al, Phys. Rev. Left. 85, 2200(2000) state complete reaction of NO conversion in N2 at formed at the interface between the silver cluster M. Lisowski et aL., AppL Phys. A 78, 165(2004) 200oC would probably be the reaction of iso- and the support, and the corresponding reaction 22. Y Bigot, V Halte, 1-C Merle, A Daunois, Chem. Phys. cyanate(which is fairly stable on alumina in the mechanism explains the key role of the size of 23.1.K Thomas, Chem. Rev. 105. 1683(2005) 24. Z -M W 1g, M. Yamaguchi, I. Goto, M. Kumagai, ntermediate step is clearly much faster than that (when performed independently that can be deduced from the data. Our me2BmbP的ECm以(m832“a,10mmcm6924 References and Notes Scheme 2 should only be regarded as the 1. Summary of Worldwide Diesel Emission Standards ments show the key role of the interface between re3(2002) ng, M Haneda, W Sun, Y Kindaichi, H. Hamada. 29. P. Bera, K C Patil, M S Hegde, Phys. Chem. Chem. Ag nanoparticles and the alumina support, the ta.49,236(200 structure of which controls the catalytic reaction. 4. H. He, Y. Yu, Catal. Today 100, 37(2005) 30. Z. P. Liu, S. ] Jenkins, D. A. King, Phys. Rev. Letf. 93, Although metal-support interactions have long 5.N. Bion, ). Saussy. M Haneda, M. Daturi, ). CataL. 217, 31. F. Thibault-Starzyk, M. Daturi, P. Bazin, 0. Marie, in been recognzed as vital for catalytic performance, 47(2003) elong, M. Datur, (Wiley-VCH, a microscopic understanding of the precise role Phys. Chem. Chem. Phys 3, 4811(2001) of the metal-support interface has emerged only 7. T.J. joi tly(30, 31). In our case, the difference be- os.47,1376(1993) 33. We thank K. Jewkes and P. Turner from Bruker Optics for tween octahedrally and tetrahedrally coordinated 9. Y. H. Yeom, H Frei, in In-Situ Spe their technical help. Supported by a fellowship from Al sites must strongly influence the reaction B. Weckhuysen, Ed. (American Sci Churchill College, Cambridge (F T.S. )and an Engineering speed. The preparation procedure and the thermal 04).pp.33-46 and Physical Sciences Research Council Advanced treatment of the solid are known to affect this 10. 5. E. Bromberg et al., Science 278, 260(1997) difference(24) 11. G. Sansone ef al. Science 314. 443(2006) 12. A. Wille, E. Fridell, AppL Catal. Environ. 70, 294(2007) The mechanism we demonstrate here is an 13. C Frischkorn, M. Wolf, Chem. Rev. 106, 4207(2006) www.sciencemag.org/cgi/content/full324/5930/1048/dc1 indication that improved catalytic activity for NO 14. 1 M Lane, D.A. King, Z. P. Liu, H Arnolds, Phys. Rev. Lett. Matenals and Methods tuning the ratio of AlI versus al with the cal.15其如 holds, D. A. King, I. M. Lane, Chem. Phys.30%面2 cination temperature of alumina. The alumina 16. G. Hoogers, D. C. Papageorgopoulos, D A. King, Surf. Sci. 26 November 2008: accepted 19 March 2009 upport has been shown to have a profound 310.147(1994) 10.1126/senc.1169041 Fabricating Genetically Engineered been constrained due to kinetic limitations, which result in poor charge-and discharge-rate capability High-Power Lithium-Ion Batteries and fading of capacity upon prolonged cycling. To address the rate limitation of these materials, most researchers have focused on tailoring particle size Using Multiple virus Genes (4, 5)to reduce both the ionic and electronic path within the particles and enhancing electronic Yun Jung Lee, Hyunjung Yi, *Woo-Jae Kim,Kisuk Kang, Dong Soo Yug e conductivity with surface carbon-coating layers Michael S Strano, Gerbrand Ceder, Angela M. Belcher (6)or conducting nanoparticles additives(7, 8). However, the fabrication of nanosized particles is Development of materials that deliver more energy at high rates is important for high-power still challenging because the materials require at pplications, including portable electronic devices and hybrid electric vehicles For lithium-ion (Li) Despite the recent advances in synthesis methods, batteries, reducing material dimensions can boost Li* ion and electron transfer in nanostructured the smallest particle size remains 20 to 40 nm(5). lectrodes. By manipulating two genes, we equipped viruses with peptide groups having affinity for Biological systems offer capabilities for en greatest affinity toward SWNTs enabled power performance of a-FePO, comparable to that or the vironmentally benign materials synthesis.An single-walled carbon nanotubes(SWNTs) on one end and peptides capable of nucleating amorphous iron phosphate(a-FePOA) fused to the viral major coat protein The virus clone with M13 virus-based biological toolkit has been crystalline lithium iron phosphate (c-LiFePOa)and showed excellent capacity retention upon cycling structures and materials(9-12). Our group has of electrodes from materials previously excluded because of extremely low electronic conductivity. Department of Materials Science and Engineering, Massachu 02139,USA ithium-ion battery electrodes store and composite electrodes (1, 2), especially for the of Technology, Cambridge, MA 02139, USA Department of release electrical energy by insertion and electrically insulating transition metal phosphate Materials Science and Engineering, Korea Advanced Institute of creasing transport of Li ions and electrons in ising Li-ion battery positive electrode materials f e and Techno gh the electrode materials. Therefore. in- based materials have elicited attentio如几m electrodes can enhance energy storage at high due to their lower toxicity, lower cost, and im- of Technology, Cambridge, MA 02139, USA. arge and dischi harge rates. Controlling nano- proved safety through improved chemical, ther- "These authors contributed equally to this work. structure has become a critical process in de- mal, and structural stability for high-power tTo whom cor veloping electrode materials to boost transport in applications(3). However, their practical use has belcher@mit.edu www.sciencemag.orgScieNceVol32422May2009 1051
shot in the 33-ns experiment. This value is much higher than rates obtained in steady-state conditions with a similar catalyst and temperature range (29). The rate-determining step in the steadystate complete reaction of NO conversion in N2 at 200°C would probably be the reaction of isocyanate (which is fairly stable on alumina in the absence of water at this temperature), and our intermediate step is clearly much faster than that (when performed independently). Scheme 2 should only be regarded as the most comprehensive version of the reaction cycle that can be deduced from the data. Our measurements show the key role of the interface between Ag nanoparticles and the alumina support, the structure of which controls the catalytic reaction. Although metal-support interactions have long been recognized as vital for catalytic performance, a microscopic understanding of the precise role of the metal-support interface has emerged only recently (30, 31). In our case, the difference between octahedrally and tetrahedrally coordinated Al sites must strongly influence the reaction speed. The preparation procedure and the thermal treatment of the solid are known to affect this difference (24). The mechanism we demonstrate here is an indication that improved catalytic activity for NO conversion could be obtained by, for instance, tuning the ratio of AlVI versus AlIV with the calcination temperature of alumina. The alumina support has been shown to have a profound influence on the dispersion of silver clusters on the catalyst (32), and catalytically active Agn + clusters form on acid sites on the alumina support. The bridged intermediate reported here can only be formed at the interface between the silver cluster and the support, and the corresponding reaction mechanism explains the key role of the size of silver clusters in catalytic activity. References and Notes 1. Summary of Worldwide Diesel Emission Standards (www.dieselnet.com/standards). 2. R. Burch, J. P. Breen, F. C. Meunier, Appl. Catal. B 39, 283 (2002). 3. F. Ouyang, M. Haneda, W. Sun, Y. Kindaichi, H. Hamada, Kinet. Catal. 49, 236 (2008). 4. H. He, Y. Yu, Catal. Today 100, 37 (2005). 5. N. Bion, J. Saussey, M. Haneda, M. Daturi, J. Catal. 217, 47 (2003). 6. N. Bion, J. Saussey, C. Hedouin, T. Seguelong, M. Daturi, Phys. Chem. Chem. Phys. 3, 4811 (2001). 7. T. J. Johnson, A. Simon, J. M. Weil, G. W. Harris, Appl. Spectrosc. 47, 1376 (1993). 8. See supporting material on Science Online. 9. Y. H. Yeom, H. Frei, in In-Situ Spectroscopy of Catalysts, B. Weckhuysen, Ed. (American Scientific, San Diego, CA, 2004), pp. 33–46. 10. S. E. Bromberg et al., Science 278, 260 (1997). 11. G. Sansone et al., Science 314, 443 (2006). 12. A. Wille, E. Fridell, Appl. Catal. Environ. 70, 294 (2007). 13. C. Frischkorn, M. Wolf, Chem. Rev. 106, 4207 (2006). 14. I. M. Lane, D. A. King, Z. P. Liu, H. Arnolds, Phys. Rev. Lett. 97, 186105 (2006). 15. H. Arnolds, D. A. King, I. M. Lane, Chem. Phys. 350, 94 (2008). 16. G. Hoogers, D. C. Papageorgopoulos, D. A. King, Surf. Sci. 310, 147 (1994). 17. W. Perrie, A. Rushton, M. Gill, P. Fox, W. O’Neill, Appl. Surf. Sci. 248, 213 (2005). 18. E. Carpene, Phys. Rev. B 74, 024301 (2006). 19. M. Bonn et al., Phys. Rev. B 61, 1101 (2000). 20. C. Voisin et al., Phys. Rev. Lett. 85, 2200 (2000). 21. M. Lisowski et al., Appl. Phys. A 78, 165 (2004). 22. Y. Bigot, V. Halté, J.-C. Merle, A. Daunois, Chem. Phys. 251, 181 (2000). 23. J. K. Thomas, Chem. Rev. 105, 1683 (2005). 24. Z.-M. Wang, M. Yamaguchi, I. Goto, M. Kumagai, Phys. Chem. Chem. Phys. 2, 3007 (2000). 25. D. F. Shriver, J. Am. Chem. Soc. 84, 4610 (1962). 26. A. Palazzi et al., J. Organomet. Chem. 689, 2324 (2004). 27. R. G. Pearson, J. Am. Chem. Soc. 85, 3533 (1963). 28. J. Sung et al., J. Phys. Chem. C 112, 5707 (2008). 29. P. Bera, K. C. Patil, M. S. Hegde, Phys. Chem. Chem. Phys. 2, 3715 (2000). 30. Z. P. Liu, S. J. Jenkins, D. A. King, Phys. Rev. Lett. 93, 156102 (2004). 31. F. Thibault-Starzyk, M. Daturi, P. Bazin, O. Marie, in Nanoparticles and Catalysis, D. Astruc, Ed. (Wiley-VCH, Weinheim, Germany, 2007), pp. 508–528. 32. K. Sato, T. Yoshinari, Y. Kintaichi, M. Haneda, H. Hamada, Appl. Catal. B 44, 67 (2003). 33. We thank K. Jewkes and P. Turner from Bruker Optics for their technical help. Supported by a fellowship from Churchill College, Cambridge (F.T.S.) and an Engineering and Physical Sciences Research Council Advanced Research Fellowship (H.A.). Supporting Online Material www.sciencemag.org/cgi/content/full/324/5930/1048/DC1 Materials and Methods SOM Text Figs. S1 and S2 References 26 November 2008; accepted 19 March 2009 10.1126/science.1169041 Fabricating Genetically Engineered High-Power Lithium-Ion Batteries Using Multiple Virus Genes Yun Jung Lee,1* Hyunjung Yi,1* Woo-Jae Kim,2 Kisuk Kang,3,4 Dong Soo Yun,1 Michael S. Strano,2 Gerbrand Ceder,1 Angela M. Belcher1,5† Development of materials that deliver more energy at high rates is important for high-power applications, including portable electronic devices and hybrid electric vehicles. For lithium-ion (Li+ ) batteries, reducing material dimensions can boost Li+ ion and electron transfer in nanostructured electrodes. By manipulating two genes, we equipped viruses with peptide groups having affinity for single-walled carbon nanotubes (SWNTs) on one end and peptides capable of nucleating amorphous iron phosphate (a-FePO4) fused to the viral major coat protein. The virus clone with the greatest affinity toward SWNTs enabled power performance of a-FePO4 comparable to that of crystalline lithium iron phosphate (c-LiFePO4) and showed excellent capacity retention upon cycling at 1C. This environmentally benign low-temperature biological scaffold could facilitate fabrication of electrodes from materials previously excluded because of extremely low electronic conductivity. Lithium-ion battery electrodes store and release electrical energy by insertion and extraction of Li+ ions and electrons through the electrode materials. Therefore, increasing transport of Li+ ions and electrons in electrodes can enhance energy storage at high charge and discharge rates. Controlling nanostructure has become a critical process in developing electrode materials to boost transport in composite electrodes (1, 2), especially for the electrically insulating transition metal phosphate cathode materials. Among them, iron phosphate– based materials have elicited attention as promising Li+ -ion battery positive electrode materials due to their lower toxicity, lower cost, and improved safety through improved chemical, thermal, and structural stability for high-power applications (3). However, their practical use has been constrained due to kinetic limitations, which result in poor charge- and discharge-rate capability and fading of capacity upon prolonged cycling. To address the rate limitation of these materials, most researchers have focused on tailoring particle size (4, 5) to reduce both the ionic and electronic path within the particles and enhancing electronic conductivity with surface carbon-coating layers (6) or conducting nanoparticles additives (7, 8). However, the fabrication of nanosized particles is still challenging because the materials require at least 350°C for crystallization and carbon coating. Despite the recent advances in synthesis methods, the smallest particle size remains 20 to 40 nm (5). Biological systems offer capabilities for environmentally benign materials synthesis. An M13 virus–based biological toolkit has been developed for the design of nanoarchitectured structures and materials (9–12). Our group has 1 Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA. 2 Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA. 3 Department of Materials Science and Engineering, Korea Advanced Institute of Science and Technology, 335, Gwahangno, Yuseong-gu, Daejeon, Korea, 305-701. 4 KAIST Institute for Eco-Energy, 335, Gwahangno, Yuseong-gu, Daejeon, Korea, 305-701. 5 Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA. *These authors contributed equally to this work. †To whom correspondence should be addressed. E-mail: belcher@mit.edu www.sciencemag.org SCIENCE VOL 324 22 MAY 2009 1051 REPORTS
REPORTS hown that Mi3 bacteriophage(phage or virus) in designing nanostructured of the protein coat(10, 12, 14). Here we dem- can be used for battery device fabrication with electrical wiring for high- onstrate a genetically programmed multifunction- improved performance by synthesizing electro- 二 bifunctionality of the virus al virus as a versatile scaffold for the synthesis and chemically active anode nanowires and organiz- Multifunctional viruses have been assembly of materials for high-power batteries. ing the virus on a polymer surface (11, 13). with desired modifications on different positions Virus-enabled nanostructured cathode mate- rials were first demonstrated by templating amor- phous anhydrous iron phosphate(a-FePOA)or the e4 virus. E4 is a modified M13 virus that has a-FePO. H-o tetraglutamate(EEEE) fused to the N terminus of each copy of pVil major coat protein. Due to the presence of extra carboxylic acid groups com- pared with wild-type M13 virus(M13KE), the E4 virus exhibits increased ionic interactions with cations and can serve as a template for terials growth (IL, 13, 15). Because only one eWeight los from virus gene(gvIll in Fig 2A)has been modified for the desired peptide motif on pIll, we call this E4 Temperature(°c) were produced on silver nanoparticles(Ag NPSh D10 loaded E4 virus. Details of the synthesis proce dure are given in the supporting online material (16). Loading of uniformly distributed Ag NPs along the coat protein of E4 virus (fig. SI)was initially intended to increase electronic conduc- tivity(7, 8, 11). The chemical analysis by direct 10C 5C 3C 2C 1CC/2 C/5C/0 current plasma atomic emission spectroscopy con- firmed the atomic ratio of Fe to P as 1: 1. Although viruses themselves have phosphate groups in their DNA (7270 phosphate groups per virus particle), 0 the fraction of phosphate groups from DNA is Specific Power(W/Kg) <1%. Figure 1A shows transmission electron Specific Capacity(mAh/g) microscope(TEM)images of a-FePO4 nanowires Fig. 1. Characterization of a-FePOa nanowire catho ith particle sizes of 10 to 20 nm in diameter les in a one-gene viral system(E4). (A) TEM imagene templated on the virus. Generally, hydrated templated a-FePOa nanowires on E4 viruses (Inset) Magnified images of the same nanowires. (B)TGA( of a-FePOa nanowires synthesized on Ag NP-loaded E4. For comparison, a tGa curve of a-F a-FePOa(a-FePOa nH2O, n=2 to 4)is preci grown on E4 virus (without Ag NPs)is also presented. (C and D)Electrochemical performance tated in aqueous solutions containing Feand ral nanowires on E4 tested between 2.0 and 4.3 V. Active materials loading was 2.63 mg/cm.(O) First PO4 around pH =7 to 8, and anhydrous ge curves at differe(m时助由4C A B Genes to b 十 High Power Lithium Ion Battery Cathode a-FePO. SWNT virus nanowire Geneticall Lescol Biomolecular recognition and attachment of templated virus to SwNT Fig. 2. Biological toolkits: genet eering and biomolecular recog- of the battery used to power a green LED The biomolecular recognition and tion. (A)A schematic presentation of the multifunctional M1 is attachment to conducting SWNT networks make efficient electrical nanoscale shown with the proteins genetically engineered in this study. Th VIll wiring to the active nanomaterials, enabling high performance. These protein (pVID, a major capsid protein of the virus, is modified to serve as a hybrid materials were assembled as a positive in a lithium-ion template for a-FePO4 growth, and the gene Ill protein (pllD is further battery using lithium metal foil as a negative to power a green ineered to have a binding affinity for SWNTS. B)A schematic diagram LED Active cathode materials loading was 3. 21 mg/cm. The 2016 Coin Cell, for fabricating genetically engineered high-power lithium-ion battery which is 2 cm in diameter and 1.6 mm in thickness, was used. LED power thodes using multifunctional viruses (two-gene system)and a photograph dissipation was 105 mw 1052 22May2009Vol324scIencEwww.sciencemag.org
shown that M13 bacteriophage (phage or virus) can be used for battery device fabrication with improved performance by synthesizing electrochemically active anode nanowires and organizing the virus on a polymer surface (11, 13). However, in designing nanostructured electrodes with better electrical wiring for high-power batteries, multifunctionality of the virus is required. Multifunctional viruses have been engineered with desired modifications on different positions of the protein coat (10, 12, 14). Here we demonstrate a genetically programmed multifunctional virus as a versatile scaffold for the synthesis and assembly of materials for high-power batteries. Virus-enabled nanostructured cathode materials were first demonstrated by templating amorphous anhydrous iron phosphate (a-FePO4) on the E4 virus. E4 is a modified M13 virus that has tetraglutamate (EEEE) fused to the N terminus of each copy of pVIII major coat protein. Due to the presence of extra carboxylic acid groups compared with wild-type M13 virus (M13KE), the E4 virus exhibits increased ionic interactions with cations and can serve as a template for materials growth (11, 13, 15). Because only one gene (gVIII in Fig. 2A) has been modified for the desired peptide motif on pVIII, we call this E4 clone a one-gene system. a-FePO4 nanowires were produced on silver nanoparticles (Ag NPs)– loaded E4 virus. Details of the synthesis procedure are given in the supporting online material (16). Loading of uniformly distributed Ag NPs along the coat protein of E4 virus (fig. S1) was initially intended to increase electronic conductivity (7, 8, 11). The chemical analysis by direct current plasma atomic emission spectroscopy confirmed the atomic ratio of Fe to P as 1:1. Although viruses themselves have phosphate groups in their DNA (7270 phosphate groups per virus particle), the fraction of phosphate groups from DNA is <1%. Figure 1A shows transmission electron microscope (TEM) images of a-FePO4 nanowires with particle sizes of 10 to 20 nm in diameter templated on the virus. Generally, hydrated a-FePO4 (a-FePO4·nH2O, n = 2 to 4) is precipitated in aqueous solutions containing Fe3+ and PO4 3− ions around pH = 7 to 8, and anhydrous structures can be obtained through the dehydration of a-FePO4·nH2O by thermal annealing at 400°C. Fig. 1. Characterization of a-FePO4 nanowire cathodes in a one-gene viral system (E4). (A) TEM images of templated a-FePO4 nanowires on E4 viruses. (Inset) Magnified images of the same nanowires. (B) TGA curve of a-FePO4 nanowires synthesized on Ag NP–loaded E4. For comparison, a TGA curve of a-FePO4·H2O grown on E4 virus (without Ag NPs) is also presented. (C and D) Electrochemical performance of a-FePO4 viral nanowires on E4 tested between 2.0 and 4.3 V. Active materials loading was 2.63 mg/cm2 . (C) First discharge curves at different rates. (D) The Ragone plot representing rate performance in terms of specific power versus specific energy (only the active electrode mass is included in the weight). Fig. 2. Biological toolkits: genetic engineering and biomolecular recognition. (A) A schematic presentation of the multifunctional M13 virus is shown with the proteins genetically engineered in this study. The gene VIII protein (pVIII), a major capsid protein of the virus, is modified to serve as a template for a-FePO4 growth, and the gene III protein (pIII) is further engineered to have a binding affinity for SWNTs. (B) A schematic diagram for fabricating genetically engineered high-power lithium-ion battery cathodes using multifunctional viruses (two-gene system) and a photograph of the battery used to power a green LED. The biomolecular recognition and attachment to conducting SWNT networks make efficient electrical nanoscale wiring to the active nanomaterials, enabling high power performance. These hybrid materials were assembled as a positive electrode in a lithium-ion battery using lithium metal foil as a negative electrode to power a green LED. Active cathode materials loading was 3.21 mg/cm2 . The 2016 Coin Cell, which is 2 cm in diameter and 1.6 mm in thickness, was used. LED power dissipation was 105 mW. 1052 22 MAY 2009 VOL 324 SCIENCE www.sciencemag.org REPORTS
Most structural water in a-FePOa'nH,O is removed Super P(TIMCAL, SUPER P Li throughout the electrodes. It is known that in from the structure around 200oC(7). Surprisingly, and polytetrafluoroethylene(PTFE) corporation of well-dispersed materials with high the viral nanowires produced on Ag NP-loaded E4 mass ratio of 70: 25: 5. Details of the conductivity and high aspect ratio leads to efficient were anhydrous as synthesized, as shown by of components are given in the sup- percolating networks(22, 23). Carbon nanotubes thermogravimetric analysis (TGA)(Fig. IB and porting online material(16). The first discharge (CNTs) have been shown to meet these needs fig S2). Without Ag NPs, nanowires have about 10 capacity at a low discharge rate of C/10(18)was (23) thus, well-dispersed single-walled CNTs eight percent (wt % structural water, which 165 mAh/g(93% of the theoretical value) and (SWNTs) in water were used. However, conven- coresponds to n= l in a-FePO4'nH2O. X-ray that of ic discharge rate was 110 mAh/g(Fig. tional composite electrode fabrication processes powder diffraction of a-FePO4 nanowires on Ag IC)(19). The rate performance is also presented inevitably suffer from aggregation of carbon NPs-loaded E4 (fig. S3A)showed only peaks as a Ragone plot(Fig. ID). In most electrode particles, thereby diminishing contact with the indexed as silver chloride(AgCi). We speculate materials, specific energy decreases substantially active materials(23). To achieve better electrical that the dehydration of FePOanH20 is related to as one applies more power(high rates), drawing wiring to our biologically derived a-FePO4,we the chlorination of Ag NPs, which could occur more current from the electrodes(20). These rate engineered a specific affinity between the con- during the incubation with the iron chloride performance values are similar to the best ducting material and active material reduced to metallic Ag after electrochemical test temperature (21). Even with this one-gene serves only as a template for a-FePO4 nanowi (fig. S3B). The reduced metallic Ag could stem, the nanostructuring of a-FePOA nano- growth, additional genetic modification was nhance local electronic conductivity as Au wires by the virus enabled an enhanced per- required to engineer the e4 virus to have a bind- tured nanowires(ID). Although the exact mech- and capacity retention upon cycling of both the Ill protein(pllm. a Is. In this context, the gene nanoparticles could in Co3 O/Au heterostruc- formance. However, high-power performance ing affinity for SWN anism of dehydration is under investigation, biologically and traditionally synthesized electro- one end of the virus(Fig. 2A), is an ideal tool be- dehydration of structural water without thermal des are still inferior to commercially available c- cause gene Ill can be controlled independently treatment was accomplished by low-temperature LiFePOa cathodes of gene VIll to insert foreign DNA encoding pIll and environmentally benign chemistry. The de Because our particles were already 10 to 20 displayed peptides. Moreover, the peptide sequene ydrated structure increases the theoretical ca- nm in diameter, our strategy for improved per- identified through the phage display with a pill pacity to 178 mAh/g, making it a good cathode formance was to increase the electronic conduc- phage-display library can be directly inserted into material ivity in the cathode by achieving better electrical the E4 virus without losing functionality (12) The electrochemical performance of viral contact between the active materials. Although Therefore, phage-display experiments to search a-FePOA nanowires as a lithium-ion battery metallic Ag NPs can locally enhance the electronic for peptide sequences with a strong binding cathode was evaluated( Fig. 1, C and D). Positive conductivity, more important for improved high- affinity for SWNTs were done first, followed by electrodes were prepared by mixing viral a- power performance is a percolating network genetic engineering into the E4 virus to produce B 250n 250nm 250nm Fig.3. Morphology of the a-FePOa grown on theD multifunctional viruses/SWNT hybrid nanostruc- tures. TEM images. (A) a-FePOa nanowires tem- plated on EC#2 viruses (before interacting with SWNTs). EC#2 virus is a two-gene system virus with the strongest binding affinity to SWNTs. B)SWNTs only(before interacting with viral a-FePOa. (C to E) SWNTS a-FePOa grown on EC#2 attached to SWNTs.(O Low magnification (x10, 000).(D)Higher magnifi- cation (x30,000).(E) High-resolution TEM(HRTEM) nages (x800,000). For HRTEM imaging, surfac tants were removed by washing with acetone. Material-specific tethering of the viral a-FePOa to the SWNTs is visualized. The amorphous nature of 4 nm FePO, was also confirmed www.sciencemag.orgScieNceVol32422May2009 1053
Most structural water in a-FePO4·nH2O is removed from the structure around 200°C (17). Surprisingly, the viral nanowires produced on Ag NP-loaded E4 were anhydrous as synthesized, as shown by thermogravimetric analysis (TGA) (Fig. 1B and fig. S2). Without Ag NPs, nanowires have about 10 weight percent (wt %) structural water, which corresponds to n = 1 in a-FePO4·nH2O. X-ray powder diffraction of a-FePO4 nanowires on Ag NPs-loaded E4 (fig. S3A) showed only peaks indexed as silver chloride (AgCl). We speculate that the dehydration of FePO4·nH2O is related to the chlorination of Ag NPs, which could occur during the incubation with the iron chloride precursor. Part of the chlorinated AgCl was reduced to metallic Ag after electrochemical test (fig. S3B). The reduced metallic Ag could enhance local electronic conductivity as Au nanoparticles could in Co3O4/Au heterostructured nanowires (11). Although the exact mechanism of dehydration is under investigation, dehydration of structural water without thermal treatment was accomplished by low-temperature and environmentally benign chemistry. The dehydrated structure increases the theoretical capacity to 178 mAh/g, making it a good cathode material. The electrochemical performance of viral a-FePO4 nanowires as a lithium-ion battery cathode was evaluated (Fig. 1, C and D). Positive electrodes were prepared by mixing viral aFePO4 with Super P (TIMCAL, SUPER P Li) carbon black and polytetrafluoroethylene (PTFE) binder in a mass ratio of 70:25:5. Details of the weight ratio of components are given in the supporting online material (16). The first discharge capacity at a low discharge rate of C/10 (18) was 165 mAh/g (93% of the theoretical value) and that of 1C discharge rate was 110 mAh/g (Fig. 1C) (19). The rate performance is also presented as a Ragone plot (Fig. 1D). In most electrode materials, specific energy decreases substantially as one applies more power (high rates), drawing more current from the electrodes (20). These rate performance values are similar to the best reported values for a-FePO4 synthesized at high temperature (21). Even with this one-gene system, the nanostructuring of a-FePO4 nanowires by the virus enabled an enhanced performance. However, high-power performance and capacity retention upon cycling of both the biologically and traditionally synthesized electrodes are still inferior to commercially available cLiFePO4 cathodes. Because our particles were already 10 to 20 nm in diameter, our strategy for improved performance was to increase the electronic conductivity in the cathode by achieving better electrical contact between the active materials. Although metallic Ag NPs can locally enhance the electronic conductivity, more important for improved highpower performance is a percolating network throughout the electrodes. It is known that incorporation of well-dispersed materials with high conductivity and high aspect ratio leads to efficient percolating networks (22, 23). Carbon nanotubes (CNTs) have been shown to meet these needs (23); thus, well-dispersed single-walled CNTs (SWNTs) in water were used. However, conventional composite electrode fabrication processes inevitably suffer from aggregation of carbon particles, thereby diminishing contact with the active materials (23). To achieve better electrical wiring to our biologically derived a-FePO4, we engineered a specific affinity between the conducting material and active material. Because the major coat protein of the E4 virus serves only as a template for a-FePO4 nanowire growth, additional genetic modification was required to engineer the E4 virus to have a binding affinity for SWNTs. In this context, the gene III protein (pIII), a minor coat protein located at one end of the virus (Fig. 2A), is an ideal tool because gene III can be controlled independently of gene VIII to insert foreign DNA encoding pIIIdisplayed peptides.Moreover, the peptide sequences identified through the phage display with a pIII phage-display library can be directly inserted into the E4 virus without losing functionality (12). Therefore, phage-display experiments to search for peptide sequences with a strong binding affinity for SWNTs were done first, followed by genetic engineering into the E4 virus to produce a Fig. 3. Morphology of the a-FePO4 grown on the multifunctional viruses/SWNT hybrid nanostructures. TEM images. (A) a-FePO4 nanowires templated on EC#2 viruses (before interacting with SWNTs). EC#2 virus is a two-gene system virus with the strongest binding affinity to SWNTs. (B) SWNTs only (before interacting with viral a-FePO4). (C to E) a-FePO4 grown on EC#2 attached to SWNTs. (C) Low magnification (×10,000). (D) Higher magnification (×30,000). (E) High-resolution TEM (HRTEM) images (×800,000). For HRTEM imaging, surfactants were removed by washing with acetone. Material-specific tethering of the viral a-FePO4 to the SWNTs is visualized. The amorphous nature of FePO4 was also confirmed. www.sciencemag.org SCIENCE VOL 324 22 MAY 2009 1053 REPORTS
REPORTS multifunctional virus structure [see Methods for tively(16). Because two genes(glll and g vill in virus were tethered to Swnts main details of the procedure(16). Several consensus Fig. 2A)were engineered with the desired modi the pill attachment; however, they made sequences were obtained from separate phage- fication on both pill and pill proteins, we called contacts with neighboring SWNTs display screening experiments. Among them, se- it a two-gene system. because of close positioning. To explore the quences N-HGHPYQHLLRVL-C(24)(named A schematic diagram for constructing the effect of specificity, we also mixed the one-gene MC#1)and N-DMPRTTMSPPPR-C(MC#2) genetically engineered high-power lithium-ion system (E4) viral nanowires solution with were selected for further experiments. The se- battery using the multifunctional two-gene virus SWNTs. Most viral a-FePOa nanowires on E4 quence MC#I started with histidine(H), whose system is illustrated in Fig. 2B. All viruses were did not make contact with SWNTs, and even if ppearance in the first position was often ob- loaded with Ag NPs to synthesize anhydrous a- they did, the contact did not seem to be due to rved in CNT-binding sequences(25). Also, it FePO4. Formation of anhydrous a-FePOA on specific binding with SWNTs (fig. S7). More- ontained several aromatic residues(H and Y), pVIll preceded the interaction with SWNTs. The over, SWNTs aggregated by themselves when which were expected to bind favorably to the synthesis procedure of anhydrous a-FePO4 nano- there was no specific binding on pill, suggesting graphene surface via T-stacking interaction(26). wires on the multifunctional viruses was the that SWNT-specific viruses enhanced dispersion The sequence MC#2 is quite different from same for growth on the one-gene system. Viral a- of SWNTs in solution. Similar observation has MC#l, and the binding affinity of clone MC#2 FePO4 solutions were then incubated with the been reported showing that SWNT-specific pep- was approximately four times as high as that of SWNT suspensions to form a-FePOwSWNTs tides can disperse SWNts, whereas nonspecific clone MC#l, whose binding affinity was already hybrid nanostructures(16). The photograph in peptides cannot (25) two-and-a-half times as high as that of wild-type Fig. 2B is the actual assembled lithium-ion The electrochemical properties of viral M13KE in the binding-affinity tests(27)(fig. S4, battery powering a light-emitting diode (led) a-FePO, SWNT hybrid materials with 5 wt A and B). The strong binding of sequence MC#2 using Li metal as a negative electrode. The virus. SWNTs were evaluated and compared(Fig 4). an be explained by the location of the hydro- enabled high-power battery could power a green Positive electrodes were prepared by mixing viral phobic segments of the sequence. The calculated LED with a small amount of active materials a-FePOSWNT hybrid composites with Super P ydrophobicity plot (fig. S5)shows a tri-block loading of 3.21 mg/cm. Although this cell was carbon black and PtFe binder in a m nass ratIo structure with hydrophilic regions on both ends assembled with lithium foil as negative electrode, 90: 5: 5(16). The addition of 5 wt extra carbon and the hydrophobic region in the middle of the we have successfully made full virus-based 3-V was used to increase the total volume, making the uence. A tri-block structure of hydrophilic- batteries with various negative electrode materi der easier to handle. without extra carbor hydrophobic-hydrophilic polymers was effective als(fig. S6). the electrodes showed slightly higher polarization when used to suspend SWNTs(25, 28). The morphology of hybrid a-FePO,/SWNT at high rates, but the difference was not sub- To genetically engineer E4 virus as a multi- nanowires on the eC#2 virus is shown in Fig 3, stantial. As demonstrated in the first discharge functional biological platform, we fused the C to E In the high-resolution TEM image(Fig. profiles(see Fig. 4A and fig. S8A for full selected sequences, MC#I and MC#2, inde- 3E), six to eight SWNTs are bundled with discharge/charge s)(19), electrochemica pendently onto the N-terminus of pill of E4 diameters of 4 to 5 nm. The TEM images show performances improve markedly as the binding virus, producing clones EC#l and EC#2, respec- that a-FePO4 nanowires templated on the multi- affinity to the SWNTs increases. Specific capac- Fig. 4. Electrochemical A 4 operties of the a-FePOa al nanowires in two- 104篇2 c/10 c/10 acity retention upon 9 cling of the a-FePOa 2C IC/2 cHic 3ci ic/ anowires/SWNTs hybrid 100150 sented. All a-FePO SWNT Specific Capacity(mAh/g) Specific Capacity(mAh/g) Specific Capacity(mAhlg hybrid materials had 5 wt c200 %/o SWNTs. EC#2 virus is a wo-gene system virus with the strongest binding affinity to SWNS; EC#1 is two-gene system vrus山 with moderate binding affinity, and E4 is a one- t- ene system virus with no o 一E4, Super P carbon insert on pilL. (A) First dis-吕 ◆EC#2 wE4, CNT.5 charge curves at different v Super P carbon 5% -Ee#50 ◆EC#1 rates. Active materials load E4 +E4 E4,234mg EC#1,231mg 102030 40 E#2,262mgm2.(B) Specific Power(W/Kg) Cycle Number higher binding affinity toward SWNTs improved rate performance due to better percolation networks than carbon black (only active electrode mass is the weight (nset) Compariso (O) Capacity retention for 50 cydes at 1C rate. There was no obvious capability of E4 virus-based ith either Super P carbon or SWNTs at least 50 cycles. Active materials loading E4, 2.90 mg/am"; EC#1, 2.22 Electrodes with well-dispersed ren with much smaller amounts. exhibited nd EC#2, 2.27 mg/am 1054 22May2009Vol324ScieNcewww.sciencemag.org
multifunctional virus structure [see Methods for details of the procedure (16)]. Several consensus sequences were obtained from separate phagedisplay screening experiments. Among them, sequences N′-HGHPYQHLLRVL-C′ (24) (named MC#1) and N′-DMPRTTMSPPPR-C′ (MC#2) were selected for further experiments. The sequence MC#1 started with histidine (H), whose appearance in the first position was often observed in CNT-binding sequences (25). Also, it contained several aromatic residues (H and Y), which were expected to bind favorably to the graphene surface via p-stacking interaction (26). The sequence MC#2 is quite different from MC#1, and the binding affinity of clone MC#2 was approximately four times as high as that of clone MC#1, whose binding affinity was already two-and-a-half times as high as that of wild-type M13KE in the binding-affinity tests (27) (fig. S4, A and B). The strong binding of sequence MC#2 can be explained by the location of the hydrophobic segments of the sequence. The calculated hydrophobicity plot (fig. S5) shows a tri-block structure with hydrophilic regions on both ends and the hydrophobic region in the middle of the sequence. A tri-block structure of hydrophilichydrophobic-hydrophilic polymers was effective when used to suspend SWNTs (25, 28). To genetically engineer E4 virus as a multifunctional biological platform, we fused the selected sequences, MC#1 and MC#2, independently onto the N-terminus of pIII of E4 virus, producing clones EC#1 and EC#2, respectively (16). Because two genes (gIII and gVIII in Fig. 2A) were engineered with the desired modification on both pIII and pVIII proteins, we called it a two-gene system. A schematic diagram for constructing the genetically engineered high-power lithium-ion battery using the multifunctional two-gene virus system is illustrated in Fig. 2B. All viruses were loaded with Ag NPs to synthesize anhydrous aFePO4. Formation of anhydrous a-FePO4 on pVIII preceded the interaction with SWNTs. The synthesis procedure of anhydrous a-FePO4 nanowires on the multifunctional viruses was the same for growth on the one-gene system. Viral aFePO4 solutions were then incubated with the SWNT suspensions to form a-FePO4/SWNTs hybrid nanostructures (16). The photograph in Fig. 2B is the actual assembled lithium-ion battery powering a light-emitting diode (LED) using Li metal as a negative electrode. The virusenabled high-power battery could power a green LED with a small amount of active materials loading of 3.21 mg/cm2 . Although this cell was assembled with lithium foil as negative electrode, we have successfully made full virus-based 3-V batteries with various negative electrode materials (fig. S6). The morphology of hybrid a-FePO4/SWNT nanowires on the EC#2 virus is shown in Fig. 3, C to E. In the high-resolution TEM image (Fig. 3E), six to eight SWNTs are bundled with diameters of 4 to 5 nm. The TEM images show that a-FePO4 nanowires templated on the multifunctional virus were tethered to SWNTs mainly through the pIII attachment; however, they made multiple contacts with neighboring SWNTs because of close positioning. To explore the effect of specificity, we also mixed the one-gene system (E4) viral nanowires solution with SWNTs. Most viral a-FePO4 nanowires on E4 did not make contact with SWNTs, and even if they did, the contact did not seem to be due to specific binding with SWNTs (fig. S7). Moreover, SWNTs aggregated by themselves when there was no specific binding on pIII, suggesting that SWNT-specific viruses enhanced dispersion of SWNTs in solution. Similar observation has been reported showing that SWNT-specific peptides can disperse SWNTs, whereas nonspecific peptides cannot (25). The electrochemical properties of viral a-FePO4/SWNT hybrid materials with 5 wt % SWNTs were evaluated and compared (Fig. 4). Positive electrodes were prepared by mixing viral a-FePO4/SWNT hybrid composites with Super P carbon black and PTFE binder in a mass ratio of 90:5:5 (16). The addition of 5 wt % extra carbon was used to increase the total volume, making the powder easier to handle. Without extra carbon, the electrodes showed slightly higher polarization at high rates, but the difference was not substantial. As demonstrated in the first discharge profiles (see Fig. 4A and fig. S8A for full discharge/charge curves) (19), electrochemical performances improve markedly as the binding affinity to the SWNTs increases. Specific capacFig. 4. Electrochemical properties ofthe a-FePO4 viral nanowires in twogene systems tested between 2.0 and 4.3 V. Rate capabilities and capacity retention upon cycling of the a-FePO4 nanowires/SWNTs hybrid electrodes templated on different clones are presented. All a-FePO4/SWNT hybrid materials had 5 wt % SWNTs. EC#2 virus is a two-gene system virus with the strongest binding affinity to SWNTs; EC#1 is a two-gene system virus with moderate binding affinity; and E4 is a onegene system virus with no insert on pIII. (A) First discharge curves at different rates. Activematerialsloading: E4, 2.34 mg/cm2 ; EC#1, 2.31 mg/cm2 ; and EC#2, 2.62 mg/cm2 . (B) Ragone plot showing improvement in high-power performance with higher binding affinity toward SWNTs (only active electrode mass is included in the weight). (Inset) Comparison of rate capability of E4 virus–based cathodes with either Super P carbon or SWNTs. Electrodes with well-dispersed SWNTs, even with much smaller amounts, exhibited improved rate performance due to better percolation networks than carbon black powders. (C) Capacity retention for 50 cycles at 1C rate. There was no obvious fading for at least 50 cycles. Active materials loading: E4, 2.90 mg/cm2 ; EC#1, 2.22 mg/cm2 ; and EC#2, 2.27 mg/cm2 . 1054 22 MAY 2009 VOL 324 SCIENCE www.sciencemag.org REPORTS
ty at a low discharge rate of c/10 increased from pecificity but depended on the random ing to the theoretical capacty of the 43 mAh/g(E4)to 160 mAh/g with EC#I and to nce of contacts between conducting net 170 mA hour/g with EC#2. The performance nd active materials. By developing a two- ell was charged at C/1o rate to 4.3 V 3 V until the current density was lower mprovement is more pronounced at higher rates. gene system with a universal handle to pick up than C100 and discharged at diff Discharge profiles of the two-gene system show electrically conducting carbon nanotubes, we 20.K Kang, Y.S. Meng, J Breger, C P. Grey, G. Ceder, much lower polarization and maintain much devised a method to realize nanoscale electrical higher capacity than those of the one-gene wiring for high-power lithium-ion batteries usin 21. Z C Shi ef al. Electrochim. Acta 53. 2665(2008) 22. S. Ahn, Electrochem. Solid-State Left. 1, 111(1998) ystem at high rates. When compared with the basic biological principles. This biological scaf- 23. 1. S. Sakamoto, B. Dunn, 1. Electrochem. Soc. 149, A26 best reported capacity for a-FePOa at a high rate fold could further extend possible sets of elec of 3C(80 mAh/g)(21), EC#2 showed a ca- trode materials by activating classes of materials 24. Abbreviations for the amino add residues are as follows pacity of 134 mAh/g, confirming substantially that have been excluded because of their ex- D, Asp: G Gly: H, His: L, Leu;M, Met; P, Pro;; Q,Gin;R, mely low electronic conducti 5. S. Wang et al., Nat. Mater. 2, 196 when we cycled EC#2 between 1.5 and 4.3 V, 6. M. Zheng et al., Science 302, 1545 the first discharge capacity at 10C reached 130 References and notes mAh/g. No published data for a-FePO4 are 1. P G. Bruce, B Scrosati, ]. M Tarascon, Angew. Chem. Int. 28. V C. Moore et al, Nano Left. 3, 1379(2003) available for comparison at rates higher than Ed47.2930(200 L Kavan, Chem. Mater. 19, 4716(2007 2. M. Armand, ]. M. Tarascon, Nature 451, 652(2008) 30. Q. Wang, N. Evans, S M. Zakeeruddin, I. Exnar 3C, but this capacity value obtained for the two- 3. S. Y. Chung, J. T. Bloking, Y. M. Chiang, Nat. Mater. 1, M. GratzeL, 1. Am. Chem. Soc. 129, 3163(2007) gene system is comparable to the capacity from 123Q002) 31. This work was supported by the Army Research Office state-of-the-art c-LiFePO4. The power perform- 4. C. Delacourt, P. Poizot, 5. Levasseur, C Masquelier, Institute of the Institute of Collaborative Biotechnologies ance of the multifunctional virus-based cathode Electrochem. Solid-State Lett 9. A352(2006) (CB)and U.S. NSF through the Materials Research was further compared with a Ragone plot. Figur 5. D. H. Kim, ]. Kim, Electrochem. Solid-State Lett. 9, A439 ateful for Ko 4B shows that two-gene system-based materials 6.).M. Tarascon et al, Dalton Trans. 2988(2004) W-).K is grateful for support from the Korea Research delivered much higher energy than the one-gene 7. F Croce et al, Electrochem. Solid-State Lett 5, A47(2002) oundation Grant funded by the Korean Government system at high power. At a specific power of Y. S. Hu et al. Adv. Mater. 19, 1963(2007) OEHRD)(KRF-2005-214-D00260) K K is grateful for 4000 W/kg(corresponding to a rate of -10C), the 9.S.R. WhaleyDSEt E.L地u,P.F. Barbara, pport from Korea Sci A M. Belcher, Nature 405, 665 (2000) rgy density of EC#l and EC#2 was two times 10. K T Nam, B.R. Peelle, s.w. Lee. A M. Belcher. Nano chnology(No. R01-2008-000-10913-0)and Energy d three times as high, respectively, as that of E4. Again, the high-power performance scales 11. K T Nam et al, Science 312, 885(2006) y(No. 2008-E-ELll-P with binding affinity. In Fig. 4B (inset), the rate 12. Y Huang et al, Nano Lett. 5, 1429(2005) 3-010). M.S.S. is grateful for funding from the NSF and performance of E4 virus-based cathodes with 13. K T Nam et al. Proc. NatL. Acad. Sci U.S_A 105. 17227 the Office of Naval Research Young Investigator Gran either Super P carbon or SWNTs was tested. ASKhalil et al., Proc. Natl. Acad. Sci. U.S.A. 104, 4892 Supporting Online Material Well-dispersed SWNTs by themselves make bet ter electrical wiring to active materials due to 15. K T. Nam, Y.L. Lee, E M. Krauland, s. T. Kottmann, Materials and Methods Figs. S1 to S8 better percolation networks than carbon black 16. Materials and methods are available as supporting powders(23), confirming the importance of nano- atena 28 January 2009: accepted 25 March 2009 scale electrical wiring. Figure 4C shows the stable 17. P. P. Prasini et al., ). Electrochem. Soc. 149, A297(2002). Published online 2 April 2009 pacity retention of a-FePOASWNT hybrid 18. Rates are reported in G-rate convention, where Cn is the 101126/science.1171541 ectrodes upon cycling at IC. Up to 50 cycles rate (current per gram) corresponding to complete Include this information when citing this paper. virtually no capacity fade was observed. A slight capacity loss after the first cycle is a characteristic cho rate again ater the sample was tested for Greater Transportation Energy iginal cpacity wasecovedconfirming srue. and GHG Offsets from Bioelectricity viral a-f ePo/ SwNT hybrid nanostructures was Than ethanol bust carbon nanotubes, leading to excellent re tention at a low SWNT content of 5 wt %.Be. J. E. campbell, 2* D. B. Lobell C.B. field4 cause the density of SWNTs is 1.33 g/cm'(23), The quantity of land available to grow biofuel crops without affecting food prices it would decrease the volumetric energy density greenhouse gas(GHG)emissions from land conversion is limited. Therefore, bioenergy should of the hybrid electrodes. However, although we maximize land-use efficiency when addressing transportation and climate change goals. Biomass nanoscale wiring by genetic engineering, we ex- these two energy pathways is not well quantified. Here, we show that bioelectricity outperforms pect that we could optimize the fraction of the ethanol across a range of feedstocks, conversion technologies, and vehicle classes. Bioelectricity conducting additives by using even better- produces an average of 81% more transportation kilometers and 108%o more emissions offsets per conducting nanowires with high aspect ratio unit area of cropland than does cellulosic ethanol. These results suggest that alternative bioenergy and higher density pathways have large differences in how efficiently they use the available land to achieve There have been efforts to electrically address transportation and climate goals electrode materials with poor electronic conduc- tivity through nanoscale wiring of active materi- Yoncems over petroleum prices and green- interest in the use of agriculture lands to gro als(8, 29, 30). However, the wiring tools used so house gas(GHG)emissions are driving energy feedstocks for these altermative transport functionalized for a single component, C research investments into altemative trans- tion technologies. Two leading technology devel- tive materials(8, 30)or conducting ma- portation technologies, but the preferred technol- opments, cellulosic ethanol and electric vehicle (29). The wiring did not completely ex- ogy is still being debated (1-5). There is surging batteries, provide altemative pathways for bioenergy www.sciencemag.orgScieNceVol32422May2009
ity at a low discharge rate of C/10 increased from 143 mAh/g (E4) to 160 mAh/g with EC#1 and to 170 mA·hour/g with EC#2. The performance improvement is more pronounced at higher rates. Discharge profiles of the two-gene system show much lower polarization and maintain much higher capacity than those of the one-gene system at high rates. When compared with the best reported capacity for a-FePO4 at a high rate of 3C (80 mAh/g) (21), EC#2 showed a capacity of 134 mAh/g, confirming substantially improved high-power performance. Moreover, when we cycled EC#2 between 1.5 and 4.3 V, the first discharge capacity at 10C reached 130 mAh/g. No published data for a-FePO4 are available for comparison at rates higher than 3C, but this capacity value obtained for the twogene system is comparable to the capacity from state-of-the-art c-LiFePO4. The power performance of the multifunctional virus-based cathode was further compared with a Ragone plot. Figure 4B shows that two-gene system–based materials delivered much higher energy than the one-gene system at high power. At a specific power of 4000 W/kg (corresponding to a rate of ~10C), the energy density of EC#1 and EC#2 was two times and three times as high, respectively, as that of E4. Again, the high-power performance scales with binding affinity. In Fig. 4B (inset), the rate performance of E4 virus–based cathodes with either Super P carbon or SWNTs was tested. Well-dispersed SWNTs by themselves make better electrical wiring to active materials due to better percolation networks than carbon black powders (23), confirming the importance of nanoscale electrical wiring. Figure 4C shows the stable capacity retention of a-FePO4/SWNT hybrid electrodes upon cycling at 1C. Up to 50 cycles, virtually no capacity fade was observed. A slight capacity loss after the first cycle is a characteristic of a-FePO4 materials (17, 21). When cycled at C/10 rate again after the sample was tested for several cycles at rates from C/10 to 10C, the original capacity was recovered, confirming structural stability (fig. S8B). Structural stability of viral a-FePO4/SWNT hybrid nanostructures was induced by materials-specific binding and stiff, robust carbon nanotubes, leading to excellent retention at a low SWNT content of 5 wt %. Because the density of SWNTs is 1.33 g/cm3 (23), it would decrease the volumetric energy density of the hybrid electrodes. However, although we adopted SWNTs to show that we can achieve nanoscale wiring by genetic engineering, we expect that we could optimize the fraction of the conducting additives by using even betterconducting nanowires with high aspect ratio and higher density. There have been efforts to electrically address electrode materials with poor electronic conductivity through nanoscale wiring of active materials (8, 29, 30). However, the wiring tools used so far were functionalized for a single component, either active materials (8, 30) or conducting materials (29). The wiring did not completely exploit specificity but depended on the random occurrence of contacts between conducting networks and active materials. By developing a twogene system with a universal handle to pick up electrically conducting carbon nanotubes, we devised a method to realize nanoscale electrical wiring for high-power lithium-ion batteries using basic biological principles. This biological scaffold could further extend possible sets of electrode materials by activating classes of materials that have been excluded because of their extremely low electronic conductivity. References and Notes 1. P. G. Bruce, B. Scrosati, J. M. Tarascon, Angew. Chem. Int. Ed. 47, 2930 (2008). 2. M. Armand, J. M. Tarascon, Nature 451, 652 (2008). 3. S. Y. Chung, J. T. Bloking, Y. M. Chiang, Nat. Mater. 1, 123 (2002). 4. C. Delacourt, P. Poizot, S. Levasseur, C. Masquelier, Electrochem. Solid-State Lett. 9, A352 (2006). 5. D. H. Kim, J. Kim, Electrochem. Solid-State Lett. 9, A439 (2006). 6. J. M. Tarascon et al., Dalton Trans. 2988 (2004). 7. F. Croce et al., Electrochem. Solid-State Lett. 5, A47 (2002). 8. Y. S. Hu et al., Adv. Mater. 19, 1963 (2007). 9. S. R. Whaley, D. S. English, E. L. Hu, P. F. Barbara, A. M. Belcher, Nature 405, 665 (2000). 10. K. T. Nam, B. R. Peelle, S. W. Lee, A. M. Belcher, Nano Lett. 4, 23 (2004). 11. K. T. Nam et al., Science 312, 885 (2006). 12. Y. Huang et al., Nano Lett. 5, 1429 (2005). 13. K. T. Nam et al., Proc. Natl. Acad. Sci. U.S.A. 105, 17227 (2008). 14. A. S. Khalil et al., Proc. Natl. Acad. Sci. U.S.A. 104, 4892 (2007). 15. K. T. Nam, Y. J. Lee, E. M. Krauland, S. T. Kottmann, A. M. Belcher, ACS Nano 2, 1480 (2008). 16. Materials and methods are available as supporting material on Science Online. 17. P. P. Prosini et al., J. Electrochem. Soc. 149, A297 (2002). 18. Rates are reported in C-rate convention, where C/n is the rate (current per gram) corresponding to complete charging or discharging to the theoretical capacity of the materials in n hours. Here, 1C corresponds to 178 mA/g. 19. In the rate test, the cell was charged at C/10 rate to 4.3 V and then held at 4.3 V until the current density was lower than C/100 and discharged at different rates. 20. K. Kang, Y. S. Meng, J. Breger, C. P. Grey, G. Ceder, Science 311, 977 (2006). 21. Z. C. Shi et al., Electrochim. Acta 53, 2665 (2008). 22. S. Ahn, Electrochem. Solid-State Lett. 1, 111 (1998). 23. J. S. Sakamoto, B. Dunn, J. Electrochem. Soc. 149, A26 (2002). 24. Abbreviations for the amino acid residues are as follows: D, Asp; G, Gly; H, His; L, Leu; M, Met; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; and Y, Tyr. 25. S. Wang et al., Nat. Mater. 2, 196 (2003). 26. M. Zheng et al., Science 302, 1545 (2003). 27. E. Ryan, U.S. patent (2002). 28. V. C. Moore et al., Nano Lett. 3, 1379 (2003). 29. L. Kavan, Chem. Mater. 19, 4716 (2007). 30. Q. Wang, N. Evans, S. M. Zakeeruddin, I. Exnar, M. Gratzel, J. Am. Chem. Soc. 129, 3163 (2007). 31. This work was supported by the Army Research Office Institute of the Institute of Collaborative Biotechnologies (ICB) and U.S. NSF through the Materials Research Science and Engineering Centers program. H.Y. is grateful for Korean Government Overseas Scholarship. W.-J.K. is grateful for support from the Korea Research Foundation Grant funded by the Korean Government (MOEHRD) (KRF-2005-214-D00260). K.K is grateful for funding support from Korea Science and Engineering Foundation of the Ministry of Education, Science and Technology (No. R01-2008-000-10913-0) and Energy Resource Technology Development program by the Ministry of Knowledge Economy (No. 2008-E-EL11-P-08- 3-010). M.S.S. is grateful for funding from the NSF and the Office of Naval Research Young Investigator Grant. Supporting Online Material www.sciencemag.org/cgi/content/full/1171541/DC1 Materials and Methods Figs. S1 to S8 References 28 January 2009; accepted 25 March 2009 Published online 2 April 2009; 10.1126/science.1171541 Include this information when citing this paper. Greater Transportation Energy and GHG Offsets from Bioelectricity Than Ethanol J. E. Campbell,1,2* D. B. Lobell,3 C. B. Field4 The quantity of land available to grow biofuel crops without affecting food prices or greenhouse gas (GHG) emissions from land conversion is limited. Therefore, bioenergy should maximize land-use efficiency when addressing transportation and climate change goals. Biomass could power either internal combustion or electric vehicles, but the relative land-use efficiency of these two energy pathways is not well quantified. Here, we show that bioelectricity outperforms ethanol across a range of feedstocks, conversion technologies, and vehicle classes. Bioelectricity produces an average of 81% more transportation kilometers and 108% more emissions offsets per unit area of cropland than does cellulosic ethanol. These results suggest that alternative bioenergy pathways have large differences in how efficiently they use the available land to achieve transportation and climate goals. Concerns over petroleum prices and greenhouse gas (GHG) emissions are driving research investments into alternative transportation technologies, but the preferred technology is still being debated (1–5). There is surging interest in the use of agriculture lands to grow energy feedstocks for these alternative transportation technologies. Two leading technology developments, cellulosic ethanol and electric vehicle batteries, provide alternative pathways for bioenergywww.sciencemag.org SCIENCE VOL 324 22 MAY 2009 1055 REPORTS
