Recent progress in oxygen-reducing laccase biocathodes for enzymatic biofuel cells

Cellular and Molecular Life Sciences

Volumn 72, Issue 5, 2015, Pages 941-952

  Le Goff, Alan ^a,b   Holzinger, Michael ^a,b   Cosnier, Serge ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

Author keywords

Biofuel cells; Electrocatalysis; Laccase; Oxygen reduction

Indexed keywords

CARBON NANOTUBE; LACCASE; OXYGEN;

BIOCATALYSIS; BIOENERGY; CHEMISTRY; ELECTRODE; METABOLISM;

BIOCATALYSIS; BIOELECTRIC ENERGY SOURCES; ELECTRODES; LACCASE; NANOTUBES, CARBON; OXYGEN;

EID: 84926677242     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1828-4     Document Type: Review

References (85)

1. Barton SC, Gallaway J, Atanassov P (2004) Enzymatic biofuel cells for implantable and microscale devices. Chem Rev 104:4867-4886. doi:10.1021/cr020719k
2. Cracknell JA, Vincent KA, Armstrong FA (2008) Enzymes as working or inspirational electrocatalysts for fuel cells and electrolysis. Chem Rev 108:2439-2461. doi:10.1021/cr0680639
3. Gellett W, Kesmez M, Schumacher J et al (2010) Biofuel cells for portable power. Electroanalysis 22:727-731. doi:10.1002/elan. 200980013
4. Willner I, Yan Y-M, Willner B, Tel-Vered R (2009) Integrated enzyme-based biofuel cells-a review. Fuel Cells 9:7-24. doi:10. 1002/fuce.200800115
5. Katz E, MacVittie K (2013) Implanted biofuel cells operating in vivo-methods, applications and perspectives-feature article. Energy Environ Sci 6:2791-2803. doi:10.1039/c3ee42126k
6. Cosnier S, Le Goff A, Holzinger M (2014) Towards glucose biofuel cells implanted in human body for powering artificial organs: review. Electrochem Commun 38:19-23. doi:10.1016/j. elecom.2013.09.021
7. Cinquin P, Gondran C, Giroud F et al (2010) A glucose biofuel cell implanted in rats. Plos One. doi:10.1371/journal.pone. 0010476 e10476
8. Zebda A, Cosnier S, Alcaraz J-P et al (2013) Single glucose biofuel cells implanted in rats power electronic devices. Sci Rep 3:1516. doi:10.1038/srep01516
9. Krishnan S, Armstrong FA (2012) Order-of-magnitude enhancement of an enzymatic hydrogen-air fuel cell based on pyrenyl carbon nanostructures. Chem Sci 3:1015-1023. doi:10. 1039/C2SC01103D
10. Ciaccafava A, De Poulpiquet A, Techer V et al (2012) An innovative powerful and mediatorless H2/O2 biofuel cell based on an outstanding bioanode. Electrochem Commun 23:25-28. doi:10.1016/j.elecom.2012.06.035
11. Addo PK, Arechederra RL, Minteer SD (2011) Towards a rechargeable alcohol biobattery. J Power Sources 196:3448-3451. doi:10.1016/j.jpowsour.2010.06.032
12. Jia W, Valdés-Ramírez G, Bandodkar AJ et al (2013) Epidermal biofuel cells: energy harvesting from human perspiration. Angew Chem Int Ed 52:7233-7236. doi:10.1002/anie.201302922
13. Solomon EI, Chen P, Metz M et al (2001) Oxygen binding, activation, and reduction to water by copper proteins. Angew Chem Int Ed 40:4570-4590. doi:10.1002/1521-3773
14. Yahiro AT, Lee SM, Kimble DO (1964) Bioelectrochemistry I. Enzyme utilizing bio-fuel cell studies. Biochim Biophys Acta 88:375-383
15. Reuillard B, Le Goff A, Agne's C et al (2013) 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 15:4892-4896. doi:10.1039/ c3cp50767j
16. Gutiérrez-Sánchez C, Pita M, Vaz-Domínguez C et al (2012) Gold nanoparticles as electronic bridges for laccase-based biocathodes. J Am Chem Soc 134:17212-17220
17. Lalaoui N, Elouarzaki K, Le Goff A et al (2013) Efficient direct oxygen reduction by laccases attached and oriented on pyrenefunctionalized polypyrrole/carbon nanotube electrodes. Chem Commun 49:9281-9283. doi:10.1039/C3CC44994G
18. Winkler JR, Gray HB (2014) Long-range electron tunneling. J Am Chem Soc 136:2930-2939. doi:10.1021/ja500215j
19. Shleev S, Tkac J, Christenson A et al (2005) Direct electron transfer between copper-containing proteins and electrodes. Biosens Bioelectron 20:2517-2554. doi:10.1016/j.bios.2004.10. 003
20. Shleev S, Jarosz-Wilkolazka A, Khalunina A et al (2005) Direct electron transfer reactions of laccases from different origins on carbon electrodes. Bioelectrochemistry 67:115-124. doi:10.1016/ j.bioelechem.2005.02.004
21. Holzinger M, Le Goff A, Cosnier S (2012) Carbon nanotube/ enzyme biofuel cells. Electrochim Acta 82:179-190. doi: 10. 1016/j.electacta.2011.12.135
22. De Poulpiquet A, Ciaccafava A, Lojou E (2014) New trends in enzyme immobilization at nanostructured interfaces for efficient electrocatalysis in biofuel cells. Electrochim Acta 126:104-114. doi:10.1016/j.electacta.2013.07.133
23. Gooding JJ, Wibowo R, Liu et al (2003) Protein electrochemistry using aligned carbon nanotube arrays. J Am Chem Soc 125:9006-9007. doi:10.1021/ja035722f
24. Wang L, Wang J, Zhou F (2004) Direct electrochemistry of catalase at a gold electrode modified with single-wall carbon nanotubes. Electroanalysis 16:627-632. doi:10.1002/elan. 200302849
25. Cai C, Chen J (2004) Direct electron transfer and bioelectrocatalysis of hemoglobin at a carbon nanotube electrode. Anal Biochem 325:285-292. doi:10.1016/j.ab.2003.10.040
26. Reuillard B, Le Goff A, Holzinger M, Cosnier S (2014) Noncovalent functionalization of carbon nanotubes with boronic acids for the wiring of glycosylated redox enzymes in oxygen-reducing biocathodes. J Mater Chem B. doi:10.1039/C3TB21846E
27. Alonso-Lomillo MA, Rüdiger O, Maroto-Valiente A et al (2007) Hydrogenase-coated carbon nanotubes for efficient H2 oxidation. Nano Lett 7:1603-1608. doi:10.1021/nl070519u
28. Hu L, Hecht DS, Grüner G (2010) Carbon nanotube thin films: fabrication, properties, and applications. Chem Rev 110:5790-5844. doi:10.1021/cr9002962
29. Fuchsberger K, Le Goff A, Gambazzi L et al (2011) Multiwalled carbon-nanotube-functionalized microelectrode arrays fabricated by microcontact printing: platform for studying chemical and electrical neuronal signaling. Small 7:524-530. doi:10.1002/smll. 201001640
30. Gooding JJ (2005) Nanostructuring electrodes with carbon nanotubes: a review on electrochemistry and applications for sensing. Electrochim Acta 50:3049-3060. doi:10.1016/j. electacta.2004.08.052
31. Hughes M, Chen GZ, Shaffer MSP et al (2002) Electrochemical capacitance of a nanoporous composite of carbon nanotubes and polypyrrole. Chem Mater 14:1610-1613. doi:10.1021/cm010744r
32. Britto PJ, Santhanam KSV, Ajayan PM (1996) Carbon nanotube electrode for oxidation of dopamine. Bioelectrochem Bioenerg 41:121-125. doi:10.1016/0302-4598(96)05078-7
33. Miyake T, Yoshino S, Yamada T et al (2011) Self-regulating enzyme-nanotube ensemble films and their application as flexible electrodes for biofuel cells. J Am Chem Soc 133:5129-5134. doi:10.1021/ja111517e
34. Zebda A, Gondran C, Le Goff A et al (2011) Mediatorless highpower glucose biofuel cells based on compressed carbon nanotube- enzyme electrodes. Nat Commun 2:370. doi:10.1038/ ncomms1365
35. Agnes C, Holzinger M, Le Goff A et al (2014) Supercapacitor/ biofuel cell hybrids based on wired enzymes on carbon nanotube matrices: autonomous reloading after high power pulses in neutral buffered glucose solutions. Energy Environ Sci 7:1884-1888. doi:10.1039/c3ee43986k
36. Deng L, Shang L, Wang Y et al (2008) Multilayer structured carbon nanotubes/poly-L-lysine/laccase composite cathode for glucose/O2 biofuel cell. Electrochem Commun 10:1012-1015. doi:10.1016/j.elecom.2008.05.001
37. Mousty C, Vieille L, Cosnier S (2007) Laccase immobilization in redox active layered double hydroxides: a reagentless amperometric biosensor. Biosens Bioelectron 22:1733-1738. doi:10. 1016/j.bios.2006.08.020
38. Deng L, Chen C, Zhou M et al (2010) Integrated self-powered microchip biosensor for endogenous biological cyanide. Anal Chem 82:4283-4287. doi:10.1021/ac100274s
39. Gellett W, Schumacher J, Kesmez M et al (2010) High current density air-breathing laccase biocathode. J Electrochem Soc 157:B557-B562. doi:10.1149/1.3309728
40. Jose Gonzalez-Guerrero M, Pablo Esquivel J, Sanchez-Molas D et al (2013) Membraneless glucose/O2 microfluidic enzymatic biofuel cell using pyrolyzed photoresist film electrodes. Lab Chip 13:2972-2979. doi:10.1039/c3lc50319d
41. Singh P, Campidelli S, Giordani S et al (2009) Organic functionalisation and characterisation of single-walled carbon nanotubes. Chem Soc Rev 38:2214-2230. doi:10.1039/ b518111a
42. Chen RJ, Zhang Y, Wang D, Dai H (2001) Noncovalent sidewall functionalization of single-walled carbon nanotubes for protein immobilization. J Am Chem Soc 123:3838-3839. doi:10.1021/ ja010172b
43. Halámková L, Halámek J, Bocharova V et al (2012) Implanted biofuel cell operating in a living snail. J Am Chem Soc 134:5040-5043. doi:10.1021/ja211714w
44. Ramasamy RP, Luckarift HR, Ivnitski DM et al (2010) High electrocatalytic activity of tethered multicopper oxidase-carbon nanotube conjugates. Chem Commun 46:6045-6047. doi:10. 1039/C0CC00911C
45. Lau C, Adkins ER, Ramasamy RP et al (2012) Design of carbon nanotube-based gas-diffusion cathode for O2 reduction by multicopper oxidases. Adv Energy Mater 2:162-168. doi:10.1002/ aenm.201100433
46. Szczupak A, Halámek J, Halámková L et al (2012) Living battery- biofuel cells operating in vivo in clams. Energy Environ Sci 5:8891-8895. doi:10.1039/C2EE21626D
47. MacVittie K, Halamek J, Halámková L et al (2012) From ''cyborg'' lobsters to a pacemaker powered by implantable biofuel cells. Energy Environ Sci 6:81-86. doi:10.1039/C2EE23209J
48. Shleev S, Pita M, Yaropolov AI et al (2006) Direct heterogeneous electron transfer reactions of Trametes hirsuta laccase at bare and thiol-modified gold electrodes. Electroanalysis 18:1901-1908. doi:10.1002/elan.200603600
49. Ciaccafava A, Infossi P, Ilbert M et al (2012) Electrochemistry, AFM, and PM-IRRA spectroscopy of immobilized hydrogenase: role of a hydrophobic helix in enzyme orientation for efficient H2 oxidation. Angew Chem Int Ed 51:953-956. doi:10.1002/anie. 201107053
50. Fowler JM, Stuart MC, Wong DKY (2008) An amperometric immunosensor with a thiolated protein G scaffold. Electrochem Commun 10:1020-1023. doi:10.1016/j.elecom.2008.05.002
51. Gutiérrez-Sánchez C, Jia W, Beyl Y et al (2012) Enhanced direct electron transfer between laccase and hierarchical carbon microfibers/ carbon nanotubes composite electrodes. Comparison of three enzyme immobilization methods. Electrochim Acta 82:218-223. doi:10.1016/j.electacta.2011.12.134
52. Blanford CF, Heath RS, Armstrong FA (2007) A stable electrode for high-potential, electrocatalytic O2 reduction based on rational attachment of a blue copper oxidase to a graphite surface. Chem Commun 17:1710. doi:10.1039/b703114a
53. Blanford CF, Foster CE, Heath RS, Armstrong FA (2008) Efficient electrocatalytic oxygen reduction by the ''blue'' copper oxidase, laccase, directly attached to chemically modified carbons. Faraday Discuss 140:319-335. doi:10.1039/B808939F
54. Stolarczyk K, Lyp D, Zelechowska K et al (2012) Arylated carbon nanotubes for biobatteries and biofuel cells. Electrochim Acta 79:74-81. doi:10.1016/j.electacta.2012.06.050
55. Karas̈kiewicz M, Nazaruk E, Želechowska K et al (2012) Fully enzymatic mediatorless fuel cell with efficient naphthylated carbon nanotube-laccase composite cathodes. Electrochem Commun 20:124-127. doi:10.1016/j.elecom.2012.04.011
56. Meredith MT, Minson M, Hickey D et al (2011) Anthracenemodified multi-walled carbon nanotubes as direct electron transfer scaffolds for enzymatic oxygen reduction. ACS Catal 1:1683-1690. doi:10.1021/cs200475q
57. Sosna M, Stoica L, Wright E et al (2012) Mass transport controlled oxygen reduction at anthraquinone modified 3D-CNT electrodes with immobilized Trametes hirsuta laccase. Phys Chem Chem Phys 14:11882. doi:10.1039/c2cp41588g
58. Bourourou M, Elouarzaki K, Lalaoui N et al (2013) Supramolecular immobilization of laccase on carbon nanotube electrodes functionalized with (methylpyrenylaminomethyl)anthraquinone for direct electron reduction of oxygen. Chem Eur J 19:9371-9375. doi:10.1002/chem.201301043
59. Cosnier S, Holzinger M (2008) Design of carbon nanotubepolymer frameworks by electropolymerization of SWCNT-pyrrole derivatives. Electrochim Acta 53:3948-3954. doi:10.1016/j. electacta.2007.10.027
60. Szot K, Nogala W, Niedziolka-Jönsson J et al (2009) Hydrophilic carbon nanoparticle-laccase thin film electrode for mediatorless dioxygen reduction: SECM activity mapping and application in zinc-dioxygen battery. Electrochim Acta 54:4620-4625. doi:10. 1016/j.electacta.2009.02.072
61. Salaj-Kosla U, Pö ller S, Schuhmann W et al (2013) Direct electron transfer of Trametes hirsuta laccase adsorbed at unmodified nanoporous gold electrodes. Bioelectrochemistry 91:15-20. doi:10.1016/j.bioelechem.2012.11.001
62. Chen T, Barton SC, Binyamin G et al (2001) A miniature biofuel cell. J Am Chem Soc 123:8630-8631. doi:10.1021/ja0163164
63. Soukharev V, Mano N, Heller A (2004) A four-electron O2- electroreduction biocatalyst superior to platinum and a biofuel cell operating at 0.88 V. J Am Chem Soc 126:8368-8369. doi:10. 1021/ja0475510
64. Kiiskinen L-L, Viikari L, Kruus K (2002) Purification and characterisation of a novel laccase from the ascomycete Melanocarpus albomyces. Appl Microbiol Biotechnol 59:198-204. doi:10.1007/s00253-002-1012-x
65. Kavanagh P, Jenkins P, Leech D (2008) Electroreduction of O2 at a mediated Melanocarpus albomyces laccase cathode in a physiological buffer. Electrochem Commun 10:970-972. doi:10.1016/ j.elecom.2008.04.025
66. Boland S, Leech D (2012) A glucose/oxygen enzymatic fuel cell based on redox polymer and enzyme immobilisation at highlyordered macroporous gold electrodes. Analyst 137:113. doi:10. 1039/c1an15537g
67. Barton SC, Kim H-H, Binyamin G et al (2001) Electroreduction of O2 to water on the ''wired'' laccase cathode. J Phys Chem B 105:11917-11921. doi:10.1021/jp012488b
68. Barton SC, Pickard M, Vazquez-Duhalt R, Heller A (2002) Electroreduction of O2 to water at 0.6 V (SHE) at pH 7 on the ''wired'' Pleurotus ostreatus laccase cathode. Biosens Bioelectron 17:1071-1074. doi:10.1016/S0956-5663(02)00100-8
69. Ackermann Y, Guschin DA, Eckhard K et al (2010) Design of a bioelectrocatalytic electrode interface for oxygen reduction in biofuel cells based on a specifically adapted Os-complex containing redox polymer with entrapped Trametes hirsuta laccase. Electrochem Commun 12:640-643. doi:10.1016/j.elecom.2010. 02.019
70. Barrie're F, Kavanagh P, Leech D (2006) A laccase-glucose oxidase biofuel cell prototype operating in a physiological buffer. Electrochim Acta 51:5187-5192. doi:10.1016/j.electacta.2006. 03.050
71. Gao F, Viry L, Maugey M et al (2010) Engineering hybrid nanotube wires for high-power biofuel cells. Nat Commun 1:2. doi:10.1038/ncomms1000
72. Beneyton T, Wijaya IPM, Salem CB et al (2013) Membraneless glucose/O2 microfluidic biofuel cells using covalently bound enzymes. Chem Commun 49:1094-1096. doi:10.1039/ C2CC37906F
73. Jenkins P, Tuurala S, Vaari A et al (2012) A comparison of glucose oxidase and aldose dehydrogenase as mediated anodes in printed glucose/oxygen enzymatic fuel cells using ABTS/laccase cathodes. Bioelectrochemistry 87:172-177. doi:10.1016/j. bioelechem.2011.11.011
74. Nazaruk E, Sadowska K, Biernat JF et al (2010) Enzymatic electrodes nanostructured with functionalized carbon nanotubes for biofuel cell applications. Anal Bioanal Chem 398:1651-1660. doi:10.1007/s00216-010-4012-1
75. Lee JY, Shin HY, Kang SW et al (2010) Use of bioelectrode containing DNA-wrapped single-walled carbon nanotubes for enzyme-based biofuel cell. J Power Sources 195:750-755. doi:10. 1016/j.jpowsour.2009.08.050
76. Bourourou M, Elouarzaki K, Holzinger M et al (2014) Freestanding redox buckypaper electrodes from multi-wall carbon nanotubes for bioelectrocatalytic oxygen reduction via mediated electron transfer. Chem Sci. doi:10.1039/C3SC53544D
77. Vaz-Dominguez C, Campuzano S, Rüdiger O et al (2008) Laccase electrode for direct electrocatalytic reduction of O2 to H2O with high-operational stability and resistance to chloride inhibition. Biosens Bioelectron 24:531-537. doi:10.1016/j.bios.2008.05.002
78. Mate DM, Gonzalez-Perez D, Falk M et al (2013) Blood tolerant laccase by directed evolution. Chem Biol 20:223-231. doi:10. 1016/j.chembiol.2013.01.001
79. Clot S, Gutierrez-Sanchez C, Shleev S et al (2012) Laccase cathode approaches to physiological conditions by local pH acidification. Electrochem Commun 18:37-40. doi:10.1016/j. elecom.2012.01.022
80. Scodeller P, Carballo R, Szamocki R et al (2010) Layer-by-layer self-assembled osmium polymer-mediated laccase oxygen cathodes for biofuel cells: the role of hydrogen peroxide. J Am Chem Soc 132:11132-11140. doi:10.1021/ja1020487
81. Milton RD, Giroud F, Thumser AE et al (2013) Hydrogen peroxide produced by glucose oxidase affects the performance of laccase cathodes in glucose/oxygen fuel cells: FAD-dependent glucose dehydrogenase as a replacement. Phys Chem Chem Phys 15:19371-19379. doi:10.1039/C3CP53351D
82. Cosnier S, Innocent C, Allien L et al (1997) An electrochemical method for making enzyme microsensors. application to the detection of dopamine and glutamate. Anal Chem 69:968-971. doi:10.1021/ac960841h
83. Castorena-Gonzalez JA, Foote C, MacVittie K et al (2013) Biofuel cell operating in vivo in rat. Electroanalysis 25:1579-1584. doi:10.1002/elan.201300136
84. Cosnier S, Holzinger M, Le Goff A, Zebda A (2012) Directtransfer biopile. WO Patent 2012022921
85. Pita M, Mate DM, Gonzalez-Perez D et al (2014) Bioelectrochemical oxidation of water. J Am Chem Soc 136:5892-5895. doi:10.1021/ja502044j