Elsevier

Biosensors and Bioelectronics

Volume 76, 15 February 2016, Pages 91-102
Biosensors and Bioelectronics

Enzymatic biofuel cells: 30 years of critical advancements

https://doi.org/10.1016/j.bios.2015.06.029Get rights and content

Highlights

  • Review of advancements in the field of enzymatic biofuel cells over the last 30 years.

  • Detailed discussion of the applications of enzymatic biofuel cells in biosensing and bioelectronics.

  • Detailed challenges for the future research and development in enzymatic biofuel cells.

Abstract

Enzymatic biofuel cells are bioelectronic devices that utilize oxidoreductase enzymes to catalyze the conversion of chemical energy into electrical energy. This review details the advancements in the field of enzymatic biofuel cells over the last 30 years. These advancements include strategies for improving operational stability and electrochemical performance, as well as device fabrication for a variety of applications, including implantable biofuel cells and self-powered sensors. It also discusses the current scientific and engineering challenges in the field that will need to be addressed in the future for commercial viability of the technology.

Introduction

One common example of a bioelectronic device is an enzymatic biofuel cell, as shown in Fig. 1. Enzymatic biofuel cells are a type of fuel cell that utilizes enzymes as the electrocatalysts to catalyze the oxidation of fuel and/or the reduction of oxygen or peroxide for energy conversion to electricity. Most traditional fuel cell electrocatalysts are conductive-metal nanoparticle catalysts that operate at temperatures ranging from 45 °C to 150 °C. These catalysts have the advantage of high stability and high activity in highly acidic and/or basic environment. However, they are plagued with passivation issues that require simple and high purity fuels (i.e. hydrogen and methanol). On the other hand, living organisms can consume and metabolize complex fuels (i.e. sucrose, fructose, etc.) and fuel mixtures and their catalysts do not have the same issues. Therefore, the field of enzymatic biofuel cells has expanded over the last 3 decades, and it is now possible to consider applications (i.e. implantable fuel cells, JP-8 fuel cells, etc.) where traditional metal nanoparticle electrocatalysts have limitations. As shown in Fig. 1, enzymatic biofuel cells are more complex than traditional fuel cells, because typically open circuit potentials are significantly lower than theoretical due to cofactor redox potentials, enzyme redox potentials, and mediator redox potentials. This review article will detail the advancements in the field of enzymatic biofuel cells over the last 30 years and discuss the challenges that will face enzymatic biofuel cell development in the next 30 years.

Section snippets

History before the debut of Biosensors & Bioelectronics

Although microbial biofuel cells have been studied for over a century, enzymatic biofuel cell history only goes back to the early 1960s. In 1964, Yahiro et al. (1964) invented the concept of enzymatic biofuel cells with a glucose oxidase bioanode and a Pt cathode. This system had very low open circuit potentials (175–350 mV), but showed the proof of concept that an oxidoreductase enzyme could catalyze a fuel cell half-reaction, in this case, the oxidation of glucose to gluconolactone, and

Cofactor regeneration

Oxidoreductase enzymes contain or require redox cofactors that change oxidation state during substrate catalysis. There are a variety of natural oxidoreductase organic and inorganic cofactors including: nicotinamide adenine dinucleotide (NAD+), nicotinamide adenine dinucleotide phosphate (NADP+), flavin adenine dinucleotide (FAD), pyrolloquinoline quinone (PQQ), hemes, iron–sulfur clusters, coenzyme Q, coenzyme F420, flavin mononucleotide (FMN) and ascorbic acid. Many of these cofactors are

Applications of enzymatic biofuel cells

There are a variety of applications for enzymatic biofuel cells. When researchers consider the low current/power density of enzymatic biofuel cells, the first application that comes to mind is powering sensors. In 2001, Katz and Willner invented the concept of self-powered biosensors that utilized a biofuel cell as a biosensor for the fuel (Katz et al., 2001). This was later translated to include inhibition and activation based self-powered biosensors (Meredith and Minteer, 2011, Wen et al.,

Challenges

Significant progress has been made in the field of biofuel cells in the last 30 years, but several issues still need to be addressed for the commercial viability of enzymatic biofuel cells for the applications discussed above. Currently, enzymatic biofuel cells are still plagued with lower than desirable stability and electrochemical performance. Performance is a vague term that can mean lower current density, power density, volumetric catalytic activity, efficiency, energy density, or open

Conclusions

Although enzymatic fuel cells predate the first issue of Biosensors & Bioelectronics, the field was very young and focused toward only mediated electron transfer. The last three decades have seen major advancements in the field to address low open circuit potentials, low current and power densities, low fuel efficiency, and low stability. These advances have resulted in open circuit potentials increasing from 175 mV to almost 1 V and current densities increasing from nA/cm2 to mA/cm2, as shown in

Acknowledgments

The authors would like to thank the National Science Foundation for funding (Grants nos.1158943 and 1057597).

References (178)

  • A. Ciaccafava et al.

    An innovative powerful and mediatorless H2/O2 biofuel cell based on an outstanding bioanode

    Electrochem. Commun.

    (2012)
  • G.P.M.K. Ciniciato et al.

    Development of paper based electrodes: from air-breathing to paintable enzymatic cathodes

    Electrochim. Acta

    (2012)
  • S. Cosnier et al.

    Towards glucose biofuel cells implanted in human body for powering artificial organs: review

    Electrochem. Commun.

    (2014)
  • L. Deng et al.

    A membraneless biofuel cell powered by ethanol and alcoholic beverage

    Biosens. Bioelectron.

    (2010)
  • S.-N. Ding et al.

    Laccase electrodes based on the combination of single-walled carbon nanotubes and redox layered double hydroxides: towards the development of biocathode for biofuel cells

    J. Power Sources

    (2010)
  • F. Durand et al.

    Designing a highly active soluble PQQ-glucose dehydrogenase for efficient glucose biosensors and biofuel cells

    Biochem. Biophys. Res. Commun.

    (2010)
  • M. Falk et al.

    Biofuel cell as a power source for electronic contact lenses

    Biosens. Bioelectron.

    (2012)
  • J. Gallaway et al.

    Oxygen-reducing enzyme cathodes produced from SLAC, a small laccase from Streptomyces coelicolor

    Biosens. Bioelectron.

    (2008)
  • F. Gao et al.

    An improved glucose/O2 membrane-less biofuel cell through glucose oxidase purification

    Biosens. Bioelectron.

    (2009)
  • F. Giroud et al.

    Anthracene-modified pyrenes immobilized on carbon nanotubes for direct electroreduction of O2 by laccase

    Electrochem. Commun.

    (2013)
  • L.T. Gorton et al.

    Electrocatalytic oxidation of reduced nicotinamide coenzymes by graphite electrodes modified with an adsorbed phenoxazinium salt, Meldola blue

    J. Electroanal. Chem. Interfacial Electrochem.

    (1984)
  • G. Gupta et al.

    Direct bio-electrocatalysis by multi-copper oxidases: gas-diffusion laccase-catalyzed cathodes for biofuel cells

    Electrochim. Acta

    (2011)
  • G. Gupta et al.

    Direct electron transfer catalyzed by bilirubin oxidase for air breathing gas-diffusion electrodes

    Electrochem. Commun.

    (2011)
  • N. Gupta et al.

    Laboratory evolution of laccase for substrate specificity

    J. Mol. Catal. B: Enzym.

    (2010)
  • L. Hussein et al.

    A highly efficient buckypaper-based electrode material for mediatorless laccase-catalyzed dioxygen reduction

    Biosens. Bioelectron.

    (2011)
  • M. Karaskiewicz et al.

    Fluoroaromatic substituents attached to carbon nanotubes help to increase oxygen concentration on biocathode in biosensors and biofuel cells

    Electrochim. Acta

    (2013)
  • M. Karaśkiewicz et al.

    Fully enzymatic mediatorless fuel cell with efficient naphthylated carbon nanotube–laccase composite cathodes

    Electrochem. Commun.

    (2012)
  • E. Katz et al.

    A non-compartmentalized glucose/O2 biofuel cell by bioengineered electrode surfaces

    J. Electroanal. Chem.

    (1999)
  • T.L. Klotzbach et al.

    Improving the microenvironment for enzyme immobilization at electrodes by hydrophobically modifying chitosan and Nafion polymers

    J. Membr. Sci.

    (2008)
  • T.L. Klotzbach et al.

    Effects of hydrophobic modification of chitosan and Nafion on transport properties, ion-exchange capacities, and enzyme immobilization

    J. Membr. Sci.

    (2006)
  • O. Kuchner et al.

    Directed evolution of enzyme catalysts

    Trends Biotechnol.

    (1997)
  • C. Laane et al.

    Use of a bioelectrochemical cell for the synthesis of (bio)chemicals

    Enzyme Microb. Technol.

    (1984)
  • Y. Li et al.

    Membraneless enzymatic biofuel cells based on multi-walled carbon nanotubes

    Int. J. Electrochem. Sci.

    (2011)
  • K.G. Lim et al.

    Microfluidic biofuel cells: the influence of electrode diffusion layer on performance

    Biosens. Bioelectron.

    (2007)
  • C. Liu et al.

    Membraneless enzymatic biofuel cells based on graphene nanosheets

    Biosens. Bioelectron.

    (2010)
  • E. Lojou

    Hydrogenases as catalysts for fuel cells: strategies for efficient immobilization at electrode interfaces

    Electrochim. Acta

    (2011)
  • N. Mano et al.

    On the parameters affecting the characteristics of the “wired” glucose oxidase anode

    Electroanal. Chem.

    (2005)
  • M. Meredith et al.

    Azine/hydrogel/nanotube composite-modified electrodes for NADH catalysis and enzyme immobilization

    Electrochim. Acta

    (2012)
  • C. Agnes et al.

    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.

    (2014)
  • L. Amir et al.

    Biofuel cell controlled by enzyme logic systems

    J. Am. Chem. Soc.

    (2009)
  • R. Arechederra et al.

    Nanomaterials in Biofuel Cells

    (2009)
  • R.L. Arechederra et al.

    Complete oxidation of glycerol in an enzymatic biofuel cell

    Fuel Cells

    (2009)
  • A. Bardea et al.

    NAD+-dependent enzyme electrodes: electrical contact of cofactor-dependent enzymes and electrodes

    J. Am. Chem. Soc.

    (1997)
  • S.C. Barton et al.

    Electroreduction of O2 to water on the “wired” laccase cathode

    J. Phys. Chem. B

    (2001)
  • A.S. Bedekar et al.

    Oxygen limitation in microfluidic biofuel cells

    Chem. Eng. Commun.

    (2008)
  • I.V. Berezin et al.

    Bioelectrocatalysis. Equilibrium oxygen potential under the laccase action

    Dokl. Akad. Nauk. USSR

    (1978)
  • S. Calabrese-Barton et al.

    Electroreduction of O2 to water on the “wired” laccase cathode

    J. Phys. Chem. B

    (2001)
  • S. Calabrese Barton et al.

    The “wired” laccase cathode: high current density electroreduction of O2 to water at +0.7 V (NHE) at pH 5

    J. Am. Chem. Soc.

    (2001)
  • E. Campbell et al.

    Enzymatic biofuel cells utilizing a biomimetic cofactor

    Chem. Commun.

    (2012)
  • A.E.G. Cass et al.

    Ferrocene-mediated enzyme electrode for amperometric determination of glucose

    Anal. Chem.

    (1984)
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