Heteroatom-doping of pristine graphene is an effective route for tailoring new characteristics in terms of catalytic performance which opens up potentials for new applications in energy conversion and storage devices. Nitrogen-doped graphene (N-graphene), for instance, has shown excellent performance in many electrochemical systems involving oxygen reduction reaction (ORR), and more recently glucose oxidation. Owing to the excellent sensitivity of N-graphene, the development of highly sensitive and fast-response enzymatic biosensors is made possible. However, a question that needs to be addressed is whether or not improving the anodic response to glucose detection leads to a higher overall performance of enzymatic biofuel cell (eBFC). Thus, here we first synthesized N-graphene via a catalyst-free single-step thermal process, and made use of it as the biocatalyst support in a membraneless eBFC to identify its role in altering the performance characteristics. Our findings demonstrate that the electron accepting nitrogen sites in the graphene structure enhances the electron transfer efficiency between the mediator (redox polymer), redox active site of the enzymes, and electrode surface. Moreover, the best performance in terms of power output and current density of eBFCs was observed when the bioanode was modified with highly doped N-graphene.
Rasmussen M, Abdellaoui S, Minteer S D. Enzymatic biofuel cells: 30 years of critical advancements. Biosensors & Bioelectronics, 2016, 76: 91–102 https://doi.org/10.1016/j.bios.2015.06.029
pmid: 26163747
Yazdi A A, D’Angelo L, Omer N, Windiasti G, Lu X, Xu J. Carbon nanotube modification of microbial fuel cell electrodes. Biosensors & Bioelectronics, 2016, 85: 536–552 https://doi.org/10.1016/j.bios.2016.05.033
pmid: 27213269
4
Pankratov D, Sundberg R, Sotres J, Maximov I, Graczyk M, Suyatin D B, González-Arribas E, Lipkin A, Montelius L, Shleev S. Transparent and flexible, nanostructured and mediatorless glucose/oxygen enzymatic fuel cells. Journal of Power Sources, 2015, 294: 501–506 https://doi.org/10.1016/j.jpowsour.2015.06.041
5
Milton R D, Lim K, Hickey D P, Minteer S D. Employing FAD-dependent glucose dehydrogenase within a glucose/oxygen enzymatic fuel cell operating in human serum. Bioelectrochemistry (Amsterdam, Netherlands), 2015, 106(Pt A): 56–63 https://doi.org/10.1016/j.bioelechem.2015.04.005
pmid: 25890695
6
Zhang L, Chen L, Zhou X, Liu Z. Towards high-voltage aqueous metal-ion batteries beyond 1.5 V: the zinc/zinc hexacyanoferrate system. Advanced Energy Materials, 2015, 5(2): 1400930 https://doi.org/10.1002/aenm.201400930
7
Ogawa Y, Takai Y, Kato Y, Kai H, Miyake T, Nishizawa M. Stretchable biofuel cell with enzyme-modified conductive textiles. Biosensors & Bioelectronics, 2015, 74: 947–952 https://doi.org/10.1016/j.bios.2015.07.063
pmid: 26257187
8
Neto S A, Milton R D, Hickey D P, Andrade A R D, Minteer S D. Membraneless enzymatic ethanol/O2 fuel cell: transitioning from an air-breathing Pt-based cathode to a bilirubin oxidase-based biocathode. Journal of Power Sources, 2016, 324: 208–214 https://doi.org/10.1016/j.jpowsour.2016.05.073
9
Qu L, Liu Y, Baek J B, Dai L. Nitrogen-doped graphene as efficient metal-free electrocatalyst for oxygen reduction in fuel cells. ACS Nano, 2010, 4(3): 1321–1326 https://doi.org/10.1021/nn901850u
pmid: 20155972
10
Ito Y, Cong W, Fujita T, Tang Z, Chen M. High catalytic activity of nitrogen and sulfur co-doped nanoporous graphene in the hydrogen evolution reaction. Angewandte Chemie International Edition, 2015, 54(7): 2131–2136 https://doi.org/10.1002/anie.201410050
pmid: 25470132
11
Lin Z, Waller G H, Liu Y, Liu M, Wong C P. Simple preparation of nanoporous few-layer nitrogen-doped graphene for use as an efficient electrocatalyst for oxygen reduction and oxygen evolution reactions. Carbon, 2013, 53: 130–136 https://doi.org/10.1016/j.carbon.2012.10.039
12
Wang H, Maiyalagan T, Wang X. Review on recent progress in nitrogen-doped graphene: synthesis, characterization, and its potential applications. ACS Catalysis, 2012, 2(5): 781–794 https://doi.org/10.1021/cs200652y
13
Wang Y, Shao Y, Matson D W, Li J, Lin Y. Nitrogen-doped graphene and its application in electrochemical biosensing. ACS Nano, 2010, 4(4): 1790–1798 https://doi.org/10.1021/nn100315s
pmid: 20373745
14
Thomas T J, Ponnusamy K E, Chang N M, Galmore K, Minteer S D. Effects of annealing on mixture-cast membranes of Nafion® and quaternary ammonium bromide salts. Journal of Membrane Science, 2003, 213(1–2): 55–66 https://doi.org/10.1016/S0376-7388(02)00512-4
15
Akers N L, Moore C M, Minteer S D. Development of alcohol/O2 biofuel cells using salt-extracted tetrabutylammonium bromide/Nafion membranes to immobilize dehydrogenase enzymes. Electrochimica Acta, 2005, 50(12): 2521–2525 https://doi.org/10.1016/j.electacta.2004.10.080
16
Dawn A, Shiraki T, Haraguchi S, Sato H, Sada K, Shinkai S. Transcription of chirality in the organogel systems dictates the enantiodifferentiating photodimerization of substituted anthracene. Chemistry (Weinheim an der Bergstrasse, Germany), 2010, 16(12): 3676–3689 https://doi.org/10.1002/chem.200902936
pmid: 20151438
17
Minson M, Meredith M T, Shrier A, Giroud F, Hickey D, Glatzhofer D T, Minteer S D. High performance glucose/O2 biofuel cell: effect of utilizing purified laccase with anthracene-modified multi-walled carbon nanotubes. Journal of the Electrochemical Society, 2012, 159(12): G166–G170 https://doi.org/10.1149/2.062212jes
18
Milton R D, Giroud F, Thumser A E, Minteer S D, Slade R C T. Bilirubin oxidase bioelectrocatalytic cathodes: the impact of hydrogen peroxide. Chemical Communications, 2014, 50(1): 94–96 https://doi.org/10.1039/C3CC47689H
pmid: 24185735
19
Merchant S A, Tran T O, Meredith M T, Cline T C, Glatzhofer D T, Schmidtke D W. High-sensitivity amperometric biosensors based on ferrocene-modified linear poly(ethylenimine). Langmuir, 2009, 25(13): 7736–7742 https://doi.org/10.1021/la9004938
pmid: 19382795
20
Merchant S A, Meredith M T, Tran T O, Brunski D B, Johnson M B, Glatzhofer D T, Schmidtke D W. Effect of mediator spacing on electrochemical and enzymatic response of ferrocene redox polymers. Journal of Physical Chemistry C, 2010, 114(26): 11627–11634 https://doi.org/10.1021/jp911188r
21
Milton R D, Giroud F, Thumser A E, Minteer S D, Slade R C T. Hydrogen peroxide produced by glucose oxidase affects the performance of laccase cathodes in glucose/oxygen fuel cells: FAD-dependent glucose dehydrogenase as a replacement. Physical Chemistry Chemical Physics, 2013, 15(44): 19371–19379 https://doi.org/10.1039/c3cp53351d
pmid: 24121716
22
Meredith M T, Kao D Y, Hickey D, Schmidtke D W, Glatzhofer D T. High current density ferrocene-modified linear poly(ethylenimine) bioanodes and their use in biofuel cells. Journal of the Electrochemical Society, 2011, 158(2): B166–B174 https://doi.org/10.1149/1.3505950
23
Lin Z, Song M K, Ding Y, Liu Y, Liu M, Wong C P. Facile preparation of nitrogen-doped graphene as a metal-free catalyst for oxygen reduction reaction. Physical Chemistry Chemical Physics, 2012, 14(10): 3381–3387 https://doi.org/10.1039/c2cp00032f
pmid: 22307527
24
Sheng Z H, Shao L, Chen J J, Bao W J, Wang F B, Xia X H. Catalyst-free synthesis of nitrogen-doped graphene via thermal annealing graphite oxide with melamine and its excellent electrocatalysis. ACS Nano, 2011, 5(6): 4350–4358 https://doi.org/10.1021/nn103584t
pmid: 21574601
25
Das A, Pisana S, Chakraborty B, Piscanec S, Saha S K, Waghmare U V, Novoselov K S, Krishnamurthy H R, Geim A K, Ferrari A C, Sood A K. Monitoring dopants by Raman scattering in an electrochemically top-gated graphene transistor. Nature Nanotechnology, 2008, 3(4): 210–215 https://doi.org/10.1038/nnano.2008.67
pmid: 18654505
26
Jia Y, Zhang L, Du A, Gao G, Chen J, Yan X, Brown C L, Yao X. Defect graphene as a trifunctional catalyst for electrochemical reactions. Advanced Materials, 2016, 28(43): 9532–9538 https://doi.org/10.1002/adma.201602912
pmid: 27622869
27
Wei D, Liu Y, Wang Y, Zhang H, Huang L, Yu G. Synthesis of N-doped graphene by chemical vapor deposition and its electrical properties. Nano Letters, 2009, 9(5): 1752–1758 https://doi.org/10.1021/nl803279t
pmid: 19326921
Zhao W, Xu J J, Shi C G, Chen H Y. Multilayer membranes via layer-by-layer deposition of organic polymer protected Prussian blue nanoparticles and glucose oxidase for glucose biosensing. Langmuir, 2005, 21(21): 9630–9634 https://doi.org/10.1021/la051370+
pmid: 16207046
30
Karyakin A A, Gitelmacher O V, Karyakina E E. Prussian blue-based first-generation biosensor. A sensitive amperometric electrode for glucose. Analytical Chemistry, 1995, 67(14): 2419–2423 https://doi.org/10.1021/ac00110a016
31
Yazdi A A, Preite R, Milton R D, Hickey D P, Minteer S D, Xu J. Rechargeable membraneless glucose biobattery: towards solid-state cathodes for implantable enzymatic devices. Journal of Power Sources, 2017, 343: 103–108 https://doi.org/10.1016/j.jpowsour.2017.01.032