Membrane/mediator-free rechargeable enzymatic biofuel cell utilizing graphene/single-wall carbon nanotube cogel electrodes

ACS Applied Materials and Interfaces

Volumn 7, Issue 7, 2015, Pages 4056-4065

  Campbell, Alan S ^a   Jeong, Yeon Joo ^a   Geier, Steven M ^a   Koepsel, Richard R ^b   Russell, Alan J ^a,b   Islam, Mohammad F ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

aerogel; biofuel cell; enzymes; glucose; graphene; single walled carbon nanotubes

Indexed keywords

AEROGELS; BIOFUELS; BIOLOGICAL FUEL CELLS; ELECTRODES; ENZYMATIC FUEL CELLS; ENZYME ELECTRODES; ENZYMES; GLUCOSE; GLUCOSE OXIDASE; GLUCOSE SENSORS; GRAPHENE; IMPLANTS (SURGICAL); NANOTUBES; OPEN CIRCUIT VOLTAGE;

BIOSENSING APPLICATIONS; ELECTRICAL CONDUCTIVITY; ELECTRON TRANSFER MEDIATORS; GLUCOSE TRANSPORT; IMPLANTABLE DEVICES; LARGE SURFACE AREA; OPERATIONAL STABILITY; SEMI-PERMEABLE MEMBRANES;

SINGLE-WALLED CARBON NANOTUBES (SWCN);

BILIRUBIN OXIDASE; BIOFUEL; CARBON NANOTUBE; GLUCOSE OXIDASE; GRAPHITE; OXIDOREDUCTASE;

BIOENERGY; CHEMISTRY; ELECTRICITY; ELECTRODE; ELECTRON TRANSPORT;

BIOELECTRIC ENERGY SOURCES; BIOFUELS; ELECTRICITY; ELECTRODES; ELECTRON TRANSPORT; GLUCOSE OXIDASE; GRAPHITE; NANOTUBES, CARBON; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS;

EID: 84923793410     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am507801x     Document Type: Article

References (76)

1. Meredith, M. T.; Minteer, S. D. Biofuel Cells: Enhanced Enzymatic Bioelectrocatalysis Annu. Rev. Anal. Chem. 2012, 5, 157-179
2. Ammam, M. Electrochemical and Electrophoretic Deposition of Enzymes: Principles, Differences and Application in Miniaturized Biosensor and Biofuel Cell Electrodes Biosens. Bioelectron. 2014, 58, 121-131
3. Leech, D.; Kavanagh, P.; Schuhmann, W. Enzymatic Fuel Cells: Recent Progress Electrochim. Acta 2012, 84, 223-234
4. de Poulpiquet, A.; Ciaccafava, A.; Lojou, E. New Trends in Enzyme Immobilization at Nanostructured Interfaces for Efficient Electrocatalysis in Biofuel Cells Electrochim. Acta 2014, 126, 104-114
5. Minteer, S. D.; Liaw, B. Y.; Cooney, M. J. Enzyme-based Biofuel Cells Curr. Opin. Biotechnol. 2007, 18, 228-234
6. Zebda, A.; Gondran, C.; Le Goff, A.; Holzinger, M.; Cinquin, P.; Cosnier, S. Mediatorless High-Power Glucose Biofuel Cells Based on Compressed Carbon Nanotube-Enzyme Electrodes Nat. Commun. 2011, 2, 370
7. Prasad, K. P.; Chen, Y.; Chen, P. Three-Dimensional Graphene-Carbon Nanotube Hybrid for High-Performance Enzymatic Biofuel Cells ACS Appl. Mater. Interfaces 2014, 6, 3387-3393
8. 2 Biofuel Cell Based on Pd Aerogels Chem.-Eur. J. 2014, 20, 4380-4385
9. So, K.; Kawai, S.; Hamano, Y.; Kitazumi, Y.; Shirai, O.; Hibi, M.; Ogawa, J.; Kano, K. Improvement of a Direct Electron Transfer-Type Fructose/Dioxygen Biofuel Cell with a Substrate-Modified Biocathode Phys. Chem. Chem. Phys. 2014, 16, 4823-4829
10. Wu, X. E.; Guo, Y. Z.; Chen, M. Y.; Chen, X. D. Fabrication of Flexible and Disposable Enzymatic Biofuel Cells Electrochim. Acta 2013, 98, 20-24
11. Miyake, T.; Haneda, K.; Yoshino, S.; Nishizawa, M. Flexible, Layered Biofuel Cells Biosens. Bioelectron. 2013, 40, 45-49
12. Das, M.; Barbora, L.; Das, P.; Goswami, P. Biofuel Cell for Generating Power from Methanol Substrate Using Alcohol Oxidase Bioanode and Air-Breathed Laccase Biocathode Biosens. Bioelectron. 2014, 59, 184-191
13. Neto, S. A.; Suda, E. L.; Xu, S.; Meredith, M. T.; De Andrade, A. R.; Minteer, S. D. Direct Electron Transfer-Based Bioanodes for Ethanol Biofuel Cells Using PQQ-Dependent Alcohol and Aldehyde Dehydrogenases Electrochim. Acta 2013, 87, 323-329
14. Arrocha, A. A.; Cano-Castillo, U.; Aguila, S. A.; Vazquez-Duhalt, R. Enzyme Orientation for Direct Electron Transfer in an Enzymatic Fuel Cell with Alcohol Oxidase and Laccase Electrodes Biosens. Bioelectron. 2014, 61, 569-574
15. Cosnier, S.; Le Goff, A.; Holzinger, M. Towards Glucose Biofuel Cells Implanted in Human Body for Powering Artificial Organs: Review Electrochem. Commun. 2014, 38, 19-23
16. Halamkova, L.; Halamek, J.; Bocharova, V.; Szczupak, A.; Alfonta, L.; Katz, E. Implanted Biofuel Cell Operating in a Living Snail J. Am. Chem. Soc. 2012, 134, 5040-5043
17. Zebda, A.; Cosnier, S.; Alcaraz, J. P.; Holzinger, M.; Le Goff, A.; Gondran, C.; Boucher, F.; Giroud, F.; Gorgy, K.; Lamraoui, H.; Cinquin, P. Single Glucose Biofuel Cells Implanted in Rats Power Electronic Devices Sci. Rep. 2013, 3, 1516
18. Falk, M.; Blum, Z.; Shleev, S. Direct Electron Transfer Based Enzymatic Fuel Cells Electrochim. Acta 2012, 82, 191-202
19. Goran, J. M.; Mantilla, S. M.; Stevenson, K. J. Influence of Surface Adsorption on the Interfacial Electron Transfer of Flavin Adenine Dinucleotide and Glucose Oxidase at Carbon Nanotube and Nitrogen-Doped Carbon Nanotube Electrodes Anal. Chem. 2013, 85, 1571-1581
20. Wohlfahrt, G.; Witt, S.; Hendle, J.; Schomburg, D.; Kalisz, H. M.; Hecht, H. J. 1.8 and 1.9 Angstrom Resolution Structures of the Penicillium Amagasakiense and Aspergillus Niger Glucose Oxidases as a Basis for Modelling Substrate Complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 1999, 55, 969-977
21. Mao, F.; Mano, N.; Heller, A. Long Tethers Binding Redox Centers to Polymer Backbones Enhance Electron Transport in Enzyme "Wiring" Hydrogels J. Am. Chem. Soc. 2003, 125, 4951-4957
22. Jenkins, P.; Tuurala, S.; Vaari, A.; Valkiainen, M.; Smolander, M.; Leech, D. A Mediated Glucose/Oxygen Enzymatic Fuel Cell Based on Printed Carbon Inks Containing Aldose Dehydrogenase and Laccase as Anode and Cathode Enzyme Microb. Technol. 2012, 50, 181-187
23. 2 Biofuel Cell and Its Operation in a Living Plant J. Am. Chem. Soc. 2003, 125, 6588-6594
24. Kim, J.; Yoo, K. H. Glucose Oxidase Nanotube-based Enzymatic Biofuel Cells with Improved Laccase Biocathodes Phys. Chem. Chem. Phys. 2013, 15, 3510-3517
25. Bunte, C.; Hussein, L.; Urban, G. A. Performance of Non-compartmentalized Enzymatic Biofuel Cell Based on Buckypaper Cathode and Ferrocene-Containing Redox Polymer Anode J. Power Sources 2014, 247, 579-586
26. Yu, Y. Y.; Chen, Z. G.; He, S. J.; Zhang, B. B.; Li, X. C.; Yao, M. C. Direct Electron Transfer of Glucose Oxidase and Biosensing for Glucose Based on PDDA-Capped Gold Nanoparticle Modified Graphene/Multi-walled Carbon Nanotubes Electrode Biosens. Bioelectron. 2014, 52, 147-152
27. Reuillard, B.; Le Goff, A.; Agnes, C.; Holzinger, M.; Zebda, A.; Gondran, C.; Elouarzaki, K.; Cosnier, S. High Power Enzymatic Biofuel Cell Based on Naphthoquinone-Mediated Oxidation of Glucose by Glucose Oxidase in a Carbon Nanotube 3d Matrix Phys. Chem. Chem. Phys. 2013, 15, 4892-4896
28. Gao, F.; Viry, L.; Maugey, M.; Poulin, P.; Mano, N. Engineering Hybrid Nanotube Wires for High-Power Biofuel Cells Nat. Commun. 2010, 1, 2
29. Deng, C. Y.; Chen, J. H.; Nie, Z.; Si, S. H. A Sensitive and Stable Biosensor Based on the Direct Electrochemistry of Glucose Oxidase Assembled Layer-by-Layer at the Multiwall Carbon Nanotube-Modified Electrode Biosens. Bioelectron. 2010, 26, 213-219
30. 2 Nanorods Synthesized by Non-Isothermal Precipitation Biosens. Bioelectron. 2012, 31, 176-181
31. Zhao, S.; Zhang, K.; Bai, Y.; Yang, W. W.; Sun, C. Q. Glucose Oxidase/Colloidal Gold Nanoparticles Immobilized in Nafion Film on Glassy Carbon Electrode: Direct Electron Transfer and Electrocatalysis Bioelectrochemistry 2006, 69, 158-163
32. Holzinger, M.; Le Goff, A.; Cosnier, S. Carbon Nanotube/Enzyme Biofuel Cells Electrochim. Acta 2012, 82, 179-190
33. Wooten, M.; Karra, S.; Zhang, M. G.; Gorski, W. On the Direct Electron Transfer, Sensing, and Enzyme Activity in the Glucose Oxidase/Carbon Nanotubes System Anal. Chem. 2014, 86, 752-757
34. Minteer, S. D.; Atanassov, P.; Luckarift, H. R.; Johnson, G. R. New Materials for Biological Fuel Cells Mater. Today 2012, 15, 166-173
35. Walcarius, A.; Minteer, S. D.; Wang, J.; Lin, Y. H.; Merkoci, A. Nanomaterials for Bio-Functionalized Electrodes: Recent Trends J. Mater. Chem. B 2013, 1, 4878-4908
36. Liang, B. G. X.; Fang, L.; Hu, Y.; Yang, G.; Zhu, Q.; Wei, J.; Ye, X. Study of Direct Electron Transfer and Enzyme Activity of Glucose Oxidase on Graphene Surface Electrochem. Commun. 2015, 50, 1-5
37. Kwon, C. H.; Lee, S. H.; Choi, Y. B.; Lee, J. A.; Kim, S. H.; Kim, H. H.; Spinks, G. M.; Wallace, G. G.; Lima, M. D.; Kozlov, M. E.; Baughman, R. H.; Kim, S. J. High-Power Biofuel Cell Textiles from Woven Biscrolled Carbon Nanotube Yarns Nat. Commun. 2014, 5, 3928
38. Kuila, T.; Bose, S.; Khanra, P.; Mishra, A. K.; Kim, N. H.; Lee, J. H. Recent Advances in Graphene-Based Biosensors Biosens. Bioelectron. 2011, 26, 4637-4648
39. 2 Biofuel Cell ACS Appl. Mater. Interfaces 2014, 6, 12808-12814
40. Brunauer, S.; Emmett, P. H.; Teller, E. Adsorption of Gases in Multimolecular Layers J. Am. Chem. Soc. 1938, 60, 309-319
41. Kim, K. H.; Oh, Y.; Islam, M. F. Mechanical and Thermal Management Characteristics of Ultrahigh Surface Area Single-Walled Carbon Nanotube Aerogels Adv. Funct. Mater. 2013, 23, 377-383
42. Kim, K. H.; Oh, Y.; Islam, M. F. Graphene Coating Makes Carbon Nanotube Aerogels Superelastic and Resistant to Fatigue Nat. Nanotechnol. 2012, 7, 562-566
43. Bryning, M. B.; Milkie, D. E.; Islam, M. F.; Hough, L. A.; Kikkawa, J. M.; Yodh, A. G. Carbon Nanotube Aerogels Adv. Mater. 2007, 19, 661-664
44. Islam, M. F.; Rojas, E.; Bergey, D. M.; Johnson, A. T.; Yodh, A. G. High Weight Fraction Surfactant Solubilization of Single-Wall Carbon Nanotubes in Water Nano Lett. 2003, 3, 269-273
45. Hummers, W. S.; Offeman, R. E. Preparation of Graphitic Oxide J. Am. Chem. Soc. 1958, 80, 1339-1339
46. Marcano, D. C.; Kosynkin, D. V.; Berlin, J. M.; Sinitskii, A.; Sun, Z. Z.; Slesarev, A.; Alemany, L. B.; Lu, W.; Tour, J. M. Improved Synthesis of Graphene Oxide ACS Nano 2010, 4, 4806-4814
47. Chen, D. T. N.; Chen, K.; Hough, L. A.; Islam, M. F.; Yodh, A. G. Rheology of Carbon Nanotube Networks During Gelation Macromolecules 2010, 43, 2048-2053
48. Hough, L. A.; Islam, M. F.; Janmey, P. A.; Yodh, A. G. Viscoelasticity of Single Wall Carbon Nanotube Suspensions Phys. Rev. Lett. 2004, 93, 168102
49. Fan, F. R. F.; Bard, A. J. Imaging of Biological Macromolecules on Mica in Humid Air by Scanning Electrochemical Microscopy Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 14222-14227
50. Gong, C.; He, Y.; Zhou, J.; Chen, W.; Han, W.; Zhang, Z.; Zhang, P.; Pan, X.; Wang, Z.; Xie, E. Synthesis on Winged Graphene Nanofibers and Their Electrochemical Capacitive Performance ACS Appl. Mater. Interfaces 2014, 6, 14844-14850
51. Heller, A. Miniature Biofuel Cells Phys. Chem. Chem. Phys. 2004, 6, 209-216
52. Rabaey, K.; Boon, N.; Siciliano, S. D.; Verhaege, M.; Verstraete, W. Biofuel Cells Select for Microbial Consortia That Self-Mediate Electron Transfer Appl. Environ. Microbiol. 2004, 70, 5373-5382
53. Campbell, A. S.; Dong, C. B.; Meng, F. K.; Hardinger, J.; Perhinschi, G.; Wu, N. Q.; Dinu, C. Z. Enzyme Catalytic Efficiency: A Function of Bio-Nano Interface Reactions ACS Appl. Mater. Interfaces 2014, 6, 5393-5403
54. Laviron, E. General Expression of the Linear Potential Sweep Voltammogram in the Case of Diffusionless Electrochemical Systems J. Electroanal. Chem. 1979, 101, 19-28
55. 2-MWCNTs as a Highly Sensitive Nano-Composite for Catalase Direct Electrochemistry Biosens. Bioelectron. 2010, 25, 1301-1306
56. Mani, V.; Devadas, B.; Chen, S. M. Direct Electrochemistry of Glucose Oxidase at Electrochemically Reduced Graphene Oxide-Multiwalled Carbon Nanotubes Hybrid Material Modified Electrode for Glucose Biosensor Biosens. Bioelectron. 2013, 41, 309-315
57. Gao, Y. F.; Yang, T.; Yang, X. L.; Zhang, Y. S.; Xiao, B. L.; Hong, J.; Sheibani, N.; Ghourchian, H.; Hong, T.; Moosavi-Movahedi, A. A. Direct Electrochemistry of Glucose Oxidase and Glucose Biosensing on a Hydroxyl Fullerenes Modified Glassy Carbon Electrode Biosens. Bioelectron. 2014, 60, 30-34
58. Razmi, H.; Mohammad-Rezaei, R. Graphene Quantum Dots as a New Substrate for Immobilization and Direct Electrochemistry of Glucose Oxidase: Application to Sensitive Glucose Determination Biosens. Bioelectron. 2013, 41, 498-504
59. Wang, J. Analytical Electrochemistry, 2 nd ed.; John Wiley & Sons: New York, 2000.
60. Brocato, S.; Lau, C.; Atanassov, P. Mechanistic Study of Direct Electron Transfer in Bilirubin Oxidase Electrochim. Acta 2012, 61, 44-49
61. 2 Reduction Dalton Trans. 2011, 40, 6668-6675
62. Ramasamy, R. P.; Luckarift, H. R.; Ivnitski, D. M.; Atanassov, P. B.; Johnson, G. R. High Electrocatalytic Activity of Tethered Multicopper Oxidase-Carbon Nanotube Conjugates Chem. Commun. 2010, 46, 6045-6047
63. Christenson, A.; Shleev, S.; Mano, N.; Heller, A.; Gorton, L. Redox Potentials of the Blue Copper Sites of Bilirubin Oxidases Biochim. Biophys. Acta, Bioenerg. 2006, 1757, 1634-1641
64. Shleev, S.; El Kasmi, A.; Ruzgas, T.; Gorton, L. Direct Heterogeneous Electron Transfer Reactions of Bilirubin Oxidase at a Spectrographic Graphite Electrode Electrochem. Commun. 2004, 6, 934-939
65. Shleev, S.; Jarosz-Wilkolazka, A.; Khalunina, A.; Morozova, O.; Yaropolov, A.; Ruzgas, T.; Gorton, L. Direct Electron Transfer Reactions of Laccases from Different Origins on Carbon Electrodes Bioelectrochemistry 2005, 67, 115-124
66. 2 based Biocathode for Applications in Glucose Biofuel Cells Biosens. Bioelectron. 2013, 39, 274-281
67. Zheng, W.; Zhao, H. Y.; Zhou, H. M.; Xu, X. X.; Ding, M. H.; Zheng, Y. F. Electrochemistry of Bilirubin Oxidase at Carbon Nanotubes J. Solid State Electrochem. 2010, 14, 249-254
68. 2 Biofuel Cell Based on Graphene and Multiwalled Carbon Nanotube Composite Modified Electrode Int. J. Electrochem. Sci. 2012, 7, 8064-8075
69. Palanisamy, S.; Cheemalapati, S.; Chen, S. M. An Enzymatic Biofuel Cell Based on Electrochemically Reduced Graphene Oxide and Multiwalled Carbon Nanotubes/Zinc Oxide Modified Electrode Int. J. Electrochem. Sci. 2012, 7, 11477-11487
70. Dudzik, J.; Chang, W. C.; Kannan, A. M.; Filipek, S.; Viswanathan, S.; Li, P. Z.; Renugopalakrishnan, V.; Audette, G. F. Cross-Linked Glucose Oxidase Clusters for Biofuel Cell Anode Catalysts Biofabrication 2013, 5, 035009
71. Shan, G. B.; Surampalli, R. Y.; Tyagi, R. D.; Zhang, T. C. Nanomaterials for Environmental Burden Reduction, Waste Treatment, and Nonpoint Source Pollution Control: A Review Front. Environ. Sci. Eng. 2009, 3, 249-264
72. Schubart, I. W.; Gobel, G.; Lisdat, F. A Pyrroloquinolinequinone-Dependent Glucose Dehydrogenase (PQQ-GDH)-Electrode with Direct Electron Transfer Based on Polyaniline Modified Carbon Nanotubes for Biofuel Cell Application Electrochim. Acta 2012, 82, 224-232
73. 2 Biofuel Cell Based on a 3-Dimensional Glucose Oxidase/SWNT/Polypyrrole Composite Electrode Biotechnol. Bioprocess Eng. 2010, 15, 371-375
74. Kwon, C. H.; Lee, S. H.; Choi, Y. B.; Lee, J. A.; Kim, S. H.; Kim, H. H.; Spinks, G. M.; Wallace, G. G.; Lima, M. D.; Kozlov, M. E.; Baughman, R. H.; Kim, S. J. High-Power Biofuel Cell Textiles from Woven Biscrolled Carbon Nanotube Yarns Nat. Commun. 2014, 5, 3928
75. 2 Biofuel Cell Electrochem. Commun. 2008, 10, 1012-1015
76. Scherbahn, V.; Putze, M. T.; Dietzel, B.; Heinlein, T.; Schneider, J. J.; Lisdat, F. Biofuel Cells Based on Direct Enzyme-Electrode Contacts Using PQQ-Dependent Glucose Dehydrogenase/Bilirubin Oxidase and Modified Carbon Nanotube Materials Biosens. Bioelectron. 2014, 61, 631-638