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Nano Research 2019, 12(4): 767-775 https://doi.org/10.1007/s12274-019-2285-z
Research Article | Issue | Published: 25 January 2019

Extending the operational lifetimes of all-direct electron transfer enzymatic biofuel cells by magnetically assembling and exchanging the active biocatalyst layers on stationary electrodes

Show Author's Information Katharina Herkendell( ),  Andreas Stemmer,  Ran Tel-Vered( )
Säumerstrasse 4, Nanotechnology Group,D-MAVT, ETH Zürich,Rüschlikon,CH-8803,Switzerland;
Keywords:
lifetime, magnetic nanoparticle, direct electron transfer, enzymatic biofuel cell, recharge, enzyme cascade
Topics:
Electron transitions Enzymatic fuel cellsEnzyme electrodesEnzymesFructoseNanomagnaticsNanoparticlesRedox reactions
Cite this article:
Herkendell K, Stemmer A, Tel-Vered R. Extending the operational lifetimes of all-direct electron transfer enzymatic biofuel cells by magnetically assembling and exchanging the active biocatalyst layers on stationary electrodes. Nano Research, 2019, 12(4): 767-775. https://doi.org/10.1007/s12274-019-2285-z
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Abstract Full text Electronic supplementary material About this article

Enzymatic biofuel cells promise green power generation from a variety of natural resources, yet these systems all suffer from time-dependent degradation effects, in particular progressing inactivation of enzymes, which severely limit the operational lifetimes of such power sources. To extend operational lifetimes, we introduce a method to magnetically exchange exhausted enzymes for fresh ones. To this end, anodic and cathodic enzymes or enzyme cascades are immobilized on carbon coated magnetic nanoparticles. Under the action of suitable magnetic field gradients, these nanoparticles are assembled on the respective stationary electrodes, or released from the electrodes for collection and subsequent exchange. We demonstrate this method on a fructose/oxygen consuming biofuel cell employing fructose dehydrogenase and bilirubin oxidase as well as on anodic and cathodic cascades employing fructose dehydrogenase/invertase and bilirubin oxidase/catalase, respectively. The enzyme-modified nanoparticles support direct electron transfer bioelectrocatalytic currents by wiring the redox active cofactors to the carbonaceous coating and from there to the electrode surfaces. The facile injection, assembly, and removal of enzyme-modified magnetic nanoparticles along with fuel solution provides a promising approach to extend the operational lifetime of enzymatic biofuel cells without the need for exchanging entire systems including chambers and electrodes.


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About this article

Extending the operational lifetimes of all-direct electron transfer enzymatic biofuel cells by magnetically assembling and exchanging the active biocatalyst layers on stationary electrodes

Show Author's information Katharina Herkendell( ), Andreas Stemmer, Ran Tel-Vered( )
Säumerstrasse 4, Nanotechnology Group,D-MAVT, ETH Zürich,Rüschlikon,CH-8803,Switzerland;

Abstract

Enzymatic biofuel cells promise green power generation from a variety of natural resources, yet these systems all suffer from time-dependent degradation effects, in particular progressing inactivation of enzymes, which severely limit the operational lifetimes of such power sources. To extend operational lifetimes, we introduce a method to magnetically exchange exhausted enzymes for fresh ones. To this end, anodic and cathodic enzymes or enzyme cascades are immobilized on carbon coated magnetic nanoparticles. Under the action of suitable magnetic field gradients, these nanoparticles are assembled on the respective stationary electrodes, or released from the electrodes for collection and subsequent exchange. We demonstrate this method on a fructose/oxygen consuming biofuel cell employing fructose dehydrogenase and bilirubin oxidase as well as on anodic and cathodic cascades employing fructose dehydrogenase/invertase and bilirubin oxidase/catalase, respectively. The enzyme-modified nanoparticles support direct electron transfer bioelectrocatalytic currents by wiring the redox active cofactors to the carbonaceous coating and from there to the electrode surfaces. The facile injection, assembly, and removal of enzyme-modified magnetic nanoparticles along with fuel solution provides a promising approach to extend the operational lifetime of enzymatic biofuel cells without the need for exchanging entire systems including chambers and electrodes.

Keywords: lifetime, magnetic nanoparticle, direct electron transfer, enzymatic biofuel cell, recharge, enzyme cascade

References(62)

1

Liu, C.; Alwarappan, S.; Chen, Z. F.; Kong, X. X.; Li, C. Z. Membraneless enzymatic biofuel cells based on graphene nanosheets. Biosens. Bioelectron. 2010, 25, 1829-1833.
DOI Google Scholar
2

Kim, R. E.; Hong, S. G.; Ha, S.; Kim, J. Enzyme adsorption, precipitation and crosslinking of glucose oxidase and laccase on polyaniline nanofibers for highly stable enzymatic biofuel cells. Enzyme Microb. Technol. 2014, 66, 35-41.
DOI Google Scholar
3

Liu, C.; Chen, Z. F.; Li, C. Z. Surface engineering of graphene-enzyme nanocomposites for miniaturized biofuel cell. IEEE Trans. Nanotechnol. 2011, 10, 59-62.
DOI Google Scholar
4

Moehlenbrock, M. J.; Minteer, S. D. Extended lifetime biofuel cells. Chem. Soc. Rev. 2008, 37, 1188-1196.
DOI Google Scholar
5

Vaddiraju, S.; Tomazos, I.; Burgess, D. J.; Jain, F. C.; Papadimitrakopoulos, F. Emerging synergy between nanotechnology and implantable biosensors: A review. Biosens. Bioelectron. 2010, 25, 1553-1565.
DOI Google Scholar
6

Rasmussen, M.; Abdellaoui, S.; Minteer, S. D. Enzymatic biofuel cells: 30 years of critical advancements. Biosens. Bioelectron. 2016, 76, 91-102.
DOI Google Scholar
7

Yang, X. Y.; Tian, G.; Jiang, N.; Su, B. L. Immobilization technology: A sustainable solution for biofuel cell design. Energy Environ. Sci. 2012, 5, 5540-5563.
DOI Google Scholar
8

Cooney, M. J.; Svoboda, V.; Lau, C.; Martin, G.; Minteer, S. D. Enzyme catalysed biofuel cells. Energy Environ. Sci. 2008, 1, 320-337.
DOI Google Scholar
9

Fischback, M. B.; Youn, J. K.; Zhao, X. Y.; Wang, P.; Park, H. G.; Chang, H. N.; Kim, J.; Ha, S. Miniature biofuel cells with improved stability under continuous operation. Electroanalysis 2006, 18, 2016-2022.
DOI Google Scholar
10

Ramanavicius, A.; Kausaite, A.; Ramanaviciene, A. Enzymatic biofuel cell based on anode and cathode powered by ethanol. Biosens. Bioelectron. 2008, 24, 761-766.
DOI Google Scholar
11

Wang, X. J.; Falk, M.; Ortiz, R.; Matsumura, H.; Bobacka, J.; Ludwig, R.; Bergelin, M.; Gorton, L.; Shleev, S. Mediatorless sugar/oxygen enzymatic fuel cells based on gold nanoparticle-modified electrodes. Biosens. Bioelectron. 2012, 31, 219-225.
DOI Google Scholar
12

MacVittie, K.; Conlon, T.; Katz, E. A wireless transmission system powered by an enzyme biofuel cell implanted in an orange. Bioelectrochemistry 2015, 106, 28-33.
DOI Google Scholar
13

Coman, V.; Vaz-Dominguez, C.; Ludwig, R.; Harreither, W.; Haltrich, D.; De Lacey, A. L.; Ruzgas, T.; Gorton, L.; Shleev, S. A membrane-, mediator-, cofactor-less glucose/oxygen biofuel cell. Phys. Chem. Chem. Phys. 2008, 10, 6093-6096.
DOI Google Scholar
14

Mazurenko, I.; Monsalve, K.; Infossi, P.; Giudici-Orticoni, M. T.; Topin, F.; Mano, N.; Lojou, E. Impact of substrate diffusion and enzyme distribution in 3D-porous electrodes: A combined electrochemical and modelling study of a thermostable H2/O2 enzymatic fuel cell. Energy Environ. Sci. 2017, 10, 1966-1982.
DOI Google Scholar
15

Shao, M. L.; Zafar, M. N.; Falk, M.; Ludwig, R.; Sygmund, C.; Peterbauer, C. K.; Guschin, D. A.; MacAodha, D.; Conghaile, P. Ó.; Leech, D. et al. Optimization of a membraneless glucose/oxygen enzymatic fuel cell based on a bioanode with high coulombic efficiency and current density. ChemPhysChem 2013, 14, 2260-2269.
DOI Google Scholar
16

Ramanavicius, A.; Kausaite, A.; Ramanaviciene, A. Biofuel cell based on direct bioelectrocatalysis. Biosens. Bioelectron. 2005, 20, 1962-1967.
DOI Google Scholar
17

Okuda, J.; Yamazaki, T.; Fukasawa, M.; Kakehi, N.; Sode, K. The application of engineered glucose dehydrogenase to a direct electron-transfer-type continuous glucose monitoring system and a compartmentless biofuel cell. Anal. Lett. 2007, 40, 431-440.
DOI Google Scholar
18

Yuhashi, N.; Tomiyama, M.; Okuda, J.; Igarashi, S.; Ikebukuro, K.; Sode, K. Development of a novel glucose enzyme fuel cell system employing protein engineered PQQ glucose dehydrogenase. Biosens. Bioelectron. 2005, 20, 2145-2150.
DOI Google Scholar
19

Rubenwolf, S.; Kerzenmacher, S.; Zengerle, R.; Von Stetten, F. Strategies to extend the lifetime of bioelectrochemical enzyme electrodes for biosensing and biofuel cell applications. Appl. Microbiol. Biotechnol. 2011, 89, 1315-1322.
DOI Google Scholar
20

Reuillard, B.; Abreu, C.; Lalaoui, N.; Le Goff, A.; Holzinger, M.; Ondel, O.; Buret, F.; Cosnier, S. One-year stability for a glucose/oxygen biofuel cell combined with pH reactivation of the laccase/carbon nanotube biocathode. Bioelectrochemistry 2015, 106, 73-76.
DOI Google Scholar
21

Miyake, T.; Oike, M.; Yoshino, S.; Yatagawa, Y.; Haneda, K.; Nishizawa, M. Automatic, sequential power generation for prolonging the net lifetime of a miniature biofuel cell stack. Lab Chip 2010, 10, 2574-2578.
DOI Google Scholar
22

Willner, I.; Yan, Y. M.; Willner, B.; Tel-Vered, R. Integrated enzyme-based biofuel cells—A review. Fuel Cells 2009, 9, 7-24.
DOI Google Scholar
23

Willner, I.; Katz, E. Magnetic control of electrocatalytic and bioelectrocatalytic processes. Angew. Chem. , Int. Ed. 2003, 42, 4576-4588.
DOI Google Scholar
24

Katz, E.; Lioubashevski, O.; Willner, I. Magnetic field effects on bioelectrocatalytic reactions of surface-confined enzyme systems: Enhanced performance of biofuel cells. J. Am. Chem. Soc. 2005, 127, 3979-3988.
DOI Google Scholar
25

Lee, J.; Lee, D.; Oh, E.; Kim, J.; Kim, Y. P.; Jin, S. M.; Kim, H. S.; Hwang, Y.; Kwak, J. H.; Park, J. G. et al. Preparation of a magnetically switchable bio-electrocatalytic system employing cross-linked enzyme aggregates in magnetic mesocellular carbon foam. Angew. Chem. 2005, 117, 7593-7598.
DOI Google Scholar
26

Wang, J.; Scampicchio, M.; Laocharoensuk, R.; Valentini, F.; González-García, O.; Burdick, J. Magnetic tuning of the electrochemical reactivity through controlled surface orientation of catalytic nanowires. J. Am. Chem. Soc. 2006, 128, 4562-4563.
DOI Google Scholar
27

Loaiza, Ó. A.; Laocharoensuk, R.; Burdick, J.; Rodríguez, M. C.; Pingarron, J. M.; Pedrero, M.; Wang, J. Adaptive orientation of multifunctional nanowires for magnetic control of bioelectrocatalytic processes. Angew. Chem. 2007, 119, 1530-1533.
DOI Google Scholar
28

Katz, E. Biofuel cells with switchable power output. Electroanalysis 2010, 22, 744-756.
DOI Google Scholar
29

Bahshi, L.; Frasconi, M.; Tel-Vered, R.; Yehezkeli, O.; Willner, I. Following the biocatalytic activities of glucose oxidase by electrochemically cross-linked enzyme-Pt nanoparticles composite electrodes. Anal. Chem. 2008, 80, 8253-8259.
DOI Google Scholar
30

Yan, Y. M.; Baravik, I.; Tel-Vered, R.; Willner, I. An ethanol/O2 biofuel cell based on an electropolymerized bilirubin oxidase/Pt nanoparticle bioelectrocatalytic O2-reduction cathode. Adv. Mater. 2009, 21, 4275-4279.
DOI Google Scholar
31

Willner, I.; Willner, B.; Tel-Vered, R. Electroanalytical applications of metallic nanoparticles and supramolecular nanostructures. Electroanalysis 2011, 23, 13-28.
DOI Google Scholar
32

Murata, K.; Kajiya, K.; Nakamura, N.; Ohno, H. Direct electrochemistry of bilirubin oxidase on three-dimensional gold nanoparticle electrodes and its application in a biofuel cell. Energy Environ. Sci. 2009, 2, 1280-1285.
DOI Google Scholar
33

Katz, E.; Willner, I.; Wang, J. Electroanalytical and bioelectroanalytical systems based on metal and semiconductor nanoparticles. Electroanalysis 2004, 16, 19-44.
DOI Google Scholar
34

Peng, H. P.; Liang, R. P.; Zhang, L.; Qiu, J. D. Facile preparation of novel core-shell enzyme-Au-polydopamine-Fe3O4 magnetic bionanoparticles for glucosesensor. Biosens. Bioelectron. 2013, 42, 293-299.
DOI Google Scholar
35

Katz, E.; Willner, I. Switching of directions of bioelectrocatalytic currents and photocurrents at electrode surfaces by using hydrophobic magnetic nanoparticles. Angew. Chem. 2005, 117, 4869-4872.
DOI Google Scholar
36

Zakharchenko, A.; Guz, N.; Laradji, A. M.; Katz, E.; Minko, S. Magnetic field remotely controlled selective biocatalysis. Nat. Catal. 2018, 1, 73-81.
DOI Google Scholar
37

Eskandari, K.; Zarei, H.; Ghourchian, H.; Amoozadeh, S. M. The electrochemical study of glucose oxidase on gold-coated magnetic iron oxide nanoparticles. J. Anal. Chem. 2015, 70, 1254-1260.
DOI Google Scholar
38

Goh, W. J.; Makam, V. S.; Hu, J.; Kang, L. F.; Zheng, M. R.; Yoong, S. L.; Udalagama, C. N. B.; Pastorin, G. Iron oxide filled magnetic carbon nanotube-enzyme conjugates for recycling of amyloglucosidase: Toward useful applications in biofuel production process. Langmuir 2012, 28, 16864-16873.
DOI Google Scholar
39

Katz, E.; Baron, R.; Willner, I. Magnetoswitchable electrochemistry gated by alkyl-chain-functionalized magnetic nanoparticles:  Control of diffusional and surface-confined electrochemical processes. J. Am. Chem. Soc. 2005, 127, 4060-4070.
DOI Google Scholar
40

Taurino, I.; Sanzò, G.; Antiochia, R.; Tortolini, C.; Mazzei, F.; Favero, G.; De Micheli, G.; Carrara, S. Recent advances in third generation biosensors based on au and pt nanostructured electrodes. TrAC Trends Anal. Chem. 2016, 79, 151-159.
DOI Google Scholar
41

Das, P.; Das, M.; Chinnadayyala, S. R.; Singha, I. M.; Goswami, P. Recent advances on developing 3rd generation enzyme electrode for biosensor applications. Biosens. Bioelectron. 2016, 79, 386-397.
DOI Google Scholar
42

Lu, X. B.; Wen, Z. H.; Li, J. H. Hydroxyl-containing antimony oxide bromide nanorods combined with chitosan for biosensors. Biomaterials 2006, 27, 5740-5747.
DOI Google Scholar
43

Zhang, Q.; Qiao, Y.; Hao, F.; Zhang, L.; Wu, S. Y.; Li, Y.; Li, J. H.; Song, X. M. Fabrication of a biocompatible and conductive platform based on a single-stranded DNA/graphene nanocomposite for direct electrochemistry and electrocatalysis. Chem. Eur. —J. 2010, 16, 8133-8139.
DOI Google Scholar
44

Milton, R. D.; Minteer, S. D. Direct enzymatic bioelectrocatalysis: Differentiating between myth and reality. J. Roy. Soc. Interface 2017, 14, 20170253.
DOI Google Scholar
45

Cosnier, S.; Gross, A. J.; Le Goff, A.; Holzinger, M. Recent advances on enzymatic glucose/oxygen and hydrogen/oxygen biofuel cells: Achievements and limitations. J. Power Sources 2016, 325, 252-263.
DOI Google Scholar
46

Falk, M.; Blum, Z.; Shleev, S. Direct electron transfer based enzymatic fuel cells. Electrochim. Acta 2012, 82, 191-202.
DOI Google Scholar
47

Wen, Z. H.; Ci, S. Q.; Hou, Y.; Chen, J. H. Facile one-pot, one-step synthesis of a carbon nanoarchitecture for an advanced multifunctonal electrocatalyst. Angew. Chem. , Int. Ed. 2014, 53, 6496-6500.
DOI Google Scholar
48

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.
DOI Google Scholar
49

Trifonov, A.; Herkendell, K.; Tel-Vered, R.; Yehezkeli, O.; Woerner, M.; Willner, I. Enzyme-capped relay-functionalized mesoporous carbon nanoparticles: Effective bioelectrocatalytic matrices for sensing and biofuel cell applications. ACS Nano 2013, 7, 11358-11368.
DOI Google Scholar
50

Taylor, A.; Krupskaya, Y.; Costa, S.; Oswald, S.; Krämer, K.; Füssel, S.; Klingeler, R.; Büchner, B.; Borowiak-Palen, E.; Wirth, M. P. Functionalization of carbon encapsulated iron nanoparticles. J. Nanopart. Res. 2010, 12, 513-519.
DOI Google Scholar
51

Ameyama, M.; Shinagawa, E.; Matsushita, K.; Adachi, O. D-fructose dehydrogenase of gluconobacter industrius: Purification, characterization, and application to enzymatic microdetermination of D-fructose. J. Bacteriol. 1981, 145, 814-823.
DOI Google Scholar
52

Herkendell, K.; Tel-Vered, R.; Stemmer, A. Switchable aerobic/anaerobic multi-substrate biofuel cell operating on anodic and cathodic enzymatic cascade assemblies. Nanoscale 2017, 9, 14118-14126.
DOI Google Scholar
53

Otsuka, K.; Sugihara, T.; Tsujino, Y.; Osakai, T.; Tamiya, E. Electrochemical consideration on the optimum ph of bilirubin oxidase. Anal. Biochem. 2007, 370, 98-106.
DOI Google Scholar
54

Trifonov, A.; Tel-Vered, R.; Fadeev, M.; Willner, I. Electrically contacted bienzyme-functionalized mesoporous carbon nanoparticle electrodes: Applications for the development of dual amperometric biosensors and multifuel-driven biofuel cells. Adv. Energy Mater. 2015, 5, 1401853.
DOI Google Scholar
55

Ramírez, P.; Mano, N.; Andreu, R.; Ruzgas, T.; Heller, A.; Gorton, L.; Shleev, S. Direct electron transfer from graphite and functionalized gold electrodes to T1 and T2/T3 copper centers of bilirubin oxidase. Biochim. Biophys. Acta 2008, 1777, 1364-1369.
DOI Google Scholar
56

Frasconi, M.; Boer, H.; Koivula, A.; Mazzei, F. Electrochemical evaluation of electron transfer kinetics of high and low redox potential laccases on gold electrode surface. Electrochim. Acta 2010, 56, 817-827.
DOI Google Scholar
57

Filip, J.; Šefčovičová, J.; Gemeiner, P.; Tkac, J. Electrochemistry of bilirubin oxidase and its use in preparation of a low cost enzymatic biofuel cell based on a renewable composite binder chitosan. Electrochim. Acta 2013, 87, 366-374.
DOI Google Scholar
58

Messiha, H. L.; Wongnate, T.; Chaiyen, P.; Jones, A. R.; Scrutton, N. S. Magnetic field effects as a result of the radical pair mechanism are unlikely in redox enzymes. J. Roy. Soc. Interface 2015, 12, 20141155.
DOI Google Scholar
59

Tsujimura, S.; Nishina, A.; Kamitaka, Y.; Kano, K. Coulometric D-fructose biosensor based on direct electron transfer using D-fructose dehydrogenase. Anal. Chem. 2009, 81, 9383-9387.
DOI Google Scholar
60

Bourdillon, C.; Demaille, C.; Moiroux, J.; Saveant, J. M. New insights into the enzymic catalysis of the oxidation of glucose by native and recombinant glucose oxidase mediated by electrochemically generated one-electron redox cosubstrates. J. Am. Chem. Soc. 1993, 115, 1-10.
DOI Google Scholar
61

Zhao, M.; Gao, Y.; Sun, J. Y.; Gao, F. Mediatorless glucose biosensor and direct electron transfer type glucose/air biofuel cell enabled with carbon nanodots. Anal. Chem. 2015, 87, 2615-2622.
DOI Google Scholar
62

Zeng, T.; Pankratov, D.; Falk, M.; Leimkühler, S.; Shleev, S.; Wollenberger, U. Miniature direct electron transfer based sulphite/oxygen enzymatic fuel cells. Biosens. Bioelectron. 2015, 66, 39-42.
DOI Google Scholar
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Publication history
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Acknowledgements

Publication history

Received: 25 October 2018
Revised: 17 December 2018
Accepted: 28 December 2018
Published: 25 January 2019
Issue date: April 2019

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Acknowledgements

Acknowledgements

Enzymatic structures were visualized with Jmol: an open-source Java viewer for chemical structures in 3D. http://www.jmol.org/.

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