CHEMELECTROCHEM
ARTICLES
DOI: 10.1002/celc.201402162
A Monosaccharide-Based Coin-Cell Biobattery
Fabien Giroud,[a] David P. Hickey,[b] David W. Schmidtke,[c] Daniel T. Glatzhofer,[b] and
Shelley D. Minteer*[a]
The utilization of carbon felt as the conductive material for the
construction of a monosaccharide-based coin-cell biobattery is
explored. Anthracene-modified carbon nanotubes were used
at the positive electrode to preferentially orientate laccase for
direct electron transfer during O2 reduction. A ferrocene-modi-
fied poly(ethylenimine) redox polymer was used to electrically
communicate with either glucose oxidase or fructose dehydro-
genase at the negative electrode. The use of carbon felt
1. Introduction
Interest in biofuel cells has grown dramatically over the last
decade.[1–3] By immobilizing oxidizing enzymes at the anode
and reducing enzymes at the cathode, a voltage can be gener-
ated that, if stacked, is sufficient to operate a wide range of
useful electronics.[4–6] However, despite a relatively large theo-
retical potential, many biofuel cells are limited by the amount
of current that can be generated due to limitations in diffusion
of either the substrate or the electrons through the electrode
material. By either vigorously stirring the solution or using a ro-
tating disk electrode, many of the substrate diffusion limita-
tions can be overcome. However, it should be noted that nei-
ther of these options is an applicable solution to the problem
of substrate diffusion, but rather a means of determining theo-
retical limitations of various biofuel-cell materials.[7] A practical
solution to the problem of electron diffusion is the use of
carbon nanotubes (CNTs) and various types of mesoporous
materials as a means of dramatically increasing the amount of
real surface area and decreasing the diffusional distances be-
tween redox species (redox mediators or active centers of en-
zymes) and electrode surfaces.[8, 9] Nonetheless, these materials
[a] Dr. F. Giroud, Prof. S. D. Minteer
Department of Chemistry, University of Utah
315 S 1400 E Rm 2020
Salt Lake City, Utah 84112 (USA)
Phone: 1-801-587-8325
E-mail: minteer@chem.utah.edu
[b] Dr. D. P. Hickey, Prof. D. T. Glatzhofer
Department of Chemistry and Biochemistry
University of Oklahoma, 101 Stephenson Parkway
Norman, Oklahoma 73019 (USA)
[c] Prof. D. W. Schmidtke
University of Oklahoma Biomedical Engineering Center
and School of Chemical, Biological, Materials Engineering
University of Oklahoma, 100 East Boyd
Norman, Oklahoma 73019 (USA)
An invited contribution to a Special Issue on Biofuel Cells
 2014 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
helped in the immobilization of a larger quantity of enzyme.
Cathodic and anodic currents with carbon felt electrodes
showed a three-fold and twofold increase, respectively, relative
to the currents obtained with Toray paper materials. Bioelec-
trodes were assembled in a commercial coin-cell battery
casing and were tested as possible biobatteries. This work
presents the first time in which a traditional battery design is
used for the performance evaluation of different biobatteries.
do not solve the substrate diffusion issue as shown in recent
papers.[10]
Much of the early work with high current density biofuel
cells has focused on the use of redox polymers to immobilize
an enzyme onto the surface of an electrode. In such electrode
films, redox mediators help shuttle electrons from the active
site of the enzyme to the electrode surface. Mediated electron
transfer is preferable for enzymes such as glucose oxidase, as
the active site resides in the interior of the enzyme, and this
makes it inaccessible for direct electron transfer to the elec-
trode surface.[11–13]
Recent research has shown that redox polymers based on
ferrocene-modified linear poly(ethylenimine) (LPEI) form hydro-
gels if crosslinked in the presence of an enzyme on the surface
of an electrode. The ferrocene–LPEI polymers interact favorably
with enzymes such as glucose oxidase through complexation
between positive charges along the polymer backbone and
the negatively charged enzyme surface, which allows for cur-
rent densities as high as 2 mA cm 2 in the presence of glucose
on planar surfaces.[14]
Unlike glucose oxidase, laccase contains a T1 Cu electron
relay that is readily accessible from the enzyme’s surface, and
it can shuttle the electrons to the active site. Work has been
done to show that anthracene-modified multiwalled CNTs (An-
MWCNTs) can bind to the active site of laccase to control the
orientation of the enzyme.[15, 16] The use of An-MWCNTs to im-
mobilize laccase allows for a very efficient means of direct elec-
tron transfer, which can result in cathodic current densities as
high as 1.84 mA cm 2 in the presence of O2.[17]
In this report, we study the use of carbon felt (CF) electrodes
as the conductive support material in place of Toray paper (TP)
electrodes for the construction of enzyme-based bioelectrodes.
For this purpose, we utilize a combination of ferrocene-modi-
fied linear poly(ethylenimine) (Fc-C6-LPEI) and glucose oxidase
(GOx) or fructose dehydrogenase (FDH) at the bioanode,
whereas an ink of An-MWCNTs and laccase is used at the cath-
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ode. Finally, we investigate a new approach for the characteri-
zation of biobatteries by sealing the bioanode and the bioca-
thode in a commercial, self-contained coin-cell design to con-
struct a monosaccharide/dioxygen biobattery. The coin-cell
battery is tested with glucose and fructose for comparison.
This work presents an attractive method to help standardize
the testing done for the performance evaluation of biobatter-
ies in development.
Materials and Methods
Materials
d-Glucose (anhydrous) was purchased from Macron Chemicals.
d-Fructose, laccase from Trametes versicolor (EC 1.10.3.2,
 10 U mg 1 solid), glucose oxidase from Aspergillus niger (EC
1.1.3.4, 192 U mg 1 solid), and horseradish peroxidase (HRP) (EC
1.11.1.7, 200–300 U mg 1 solid) were purchased from Sigma–Al-
drich. Fructose dehydrogenase from Gluconobacter sp. (EC
1.1.99.11, Grade III, 169 U mg 1 of solid) was purchased from
Toyobo Enzymes. Ethylene glycol diglycidyl ether (EGDGE) was pur-
chased from Polysciences, Inc., Washington, PA. All chemicals used
in the synthesis of the redox polymer were purchased from
Sigma–Aldrich and were used as received unless otherwise noted.
Ferrocene-modified linear poly(ethyleneimine) (Fc-C6-LPEI) was syn-
thesized as previously reported.[18] Stock solutions of glucose and
fructose were allowed to mutarotate overnight at 4 8C. TP electro-
des were purchased from Fuel Cell Earth (non-wet proof, Prod. No.
TGP-H-060). CF was obtained from Alfa Aesar (3.18 mm thick,
99.0 %). Coin-cell casings were obtained from AA Portable Power
Corp (CR2032, cases-304). The insulator layer between the anode
and cathode was made of filter paper from Whatman (diameter =
70 mm. MWCNTs were purchased from cheaptubes.com (outer di-
ameter = 10-20 nm, length = 10–30 mm) and were used as received.
The anthracene (An)-modified MWCNTs were synthesized accord-
ing to our previous work.[15] In brief, hydroxylated MWCNTs (OH
group 1.76 wt %) were dispersed in acetonitrile for 15 min. Anthra-
cene-2-carbonyl chloride (1.0 equiv. of OH group) was added to
the mixture, and the solution was vigorously stirred and heated at
reflux overnight. The modified CNTs were filtered and washed with
copious amounts of acetonitrile, benzene, and dichloromethane to
remove any unreacted starting materials.
Electrode Fabrication
Biocathode preparation: For 1 cm2 TP electrode modification, An-
MWCNTs (7.5 mg) were dispersed in a laccase solution (75 mL,
40 mg mL 1, 50 mm citrate buffer, pH 5.0) by successive sonication
and vortexing (1 min each, repeated 4 ). A tetrabutylammonium
bromide modified Nafion (TBAB-Nafion) suspension (25 mL of a 5 %
by wt suspension) as previously described was used as an immobi-
lizing agent and was added to the solution.[19] The mixture was
mixed by vortex and sonication (1 min each). The resulting black
ink was paint coated evenly on four TP electrodes. Unless other-
wise specified in the text, the same preparation was used to
modify a single electrode for 1 cm2 CF electrodes. The CF was not
treated before coating with the bioink and was used dry.
Bioanode preparation: For 1 cm2 TP electrode modification or CF
electrodes, a freshly dispersed solution of CNTs in deionized water
(34.4 mL, 1 mg mL 1) was added to Fc-C6-LPEI (120 mL, 12 mg mL 1
in deionized water), and the mixture was sonicated and vortexed
(1 min each, solution 1). For single enzyme bioelectrodes, oxidore-
 2014 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
www.chemelectrochem.org
ductase (17.2 mL, 13 mg mL 1) was added to solution 1, and the so-
lution was mixed by vortexing for 1 min. Finally, a solution of 4.3 %
EGDGE (6.44 mL, EGDGE/water = 2:45 v/v) was added to the previ-
ous mixture. The resulting solution was mixed thoroughly. The TP
and CF electrodes were modified by dropcasting from the final so-
lution (25 and 50 mL, respectively), and the resulting films were al-
lowed to dry in open air at room temperature overnight to ensure
crosslinking. In the case of the CF electrodes, the felt was thor-
oughly soaked in deionized water to help the hydrogel to diffuse
inside the pores.
Voltammetric and Amperometric Characterization of Half-
Cell Biocathodes and Bioanodes
Biocathodes: Half-cell electrodes were tested by using a three-elec-
trode setup. Cyclic voltammetry (CV) experiments were performed
on both TP and CF 1 cm  1 cm electrodes as the working elec-
trode. The potential was scanned from 0.7 to 0.0 V versus a saturat-
ed calomel electrode (SCE) by using a platinum mesh counter elec-
trode at 1 mV s 1. Experiments were performed in 50 mm citrate
buffer at pH 4.5 (unless otherwise stated) by using a DY2300 po-
tentiostat (Digi Ivy, TX USA). Each experiment was performed in
triplicate by using separate electrodes (n = 3) in dissolved O2 or in
pure O2 saturated conditions. Electrodes were allowed to equili-
brate for 5 min in buffer before performing CV experiments.
Amperometric experiments were performed by applying 0.3 V
versus SCE for 23 h in dissolved O2 without any stirring and at
room temperature (22  2 8C). CV and amperometric testing was
performed for 7 days to assess the stability of the biocathode.
Bioanodes: Half-cell electrodes were tested by using a three-elec-
trode setup. Electrodes were allowed to equilibrate for 5 min in
buffer before performing the CV experiments to determine the oxi-
dation potential for the redox hydrogel on both the TP and CF
1 cm  1 cm electrodes. The potential was scanned from 0.1 to
0.6 V versus SCE by using a platinum mesh counter electrode at
20 mV s 1. Experiments were performed in 50 mm citrate buffer at
pH 5.0 by using a DY2300 potentiostat (Digi Ivy, TX USA). Each ex-
periment was performed in triplicate by using separate electrodes
(n = 3). Afterwards, amperometric studies were performed by al-
lowing the films to reach a steady-state current at a potential E
that was 50 mV above the peak oxidation potential (Epa) at 25 8C
(i.e. E = Epa + 50 mV). The solutions were continuously stirred at
400 rpm. After the charging current dissipated (t = 1000 s), sequen-
tial injections of a 1 m substrate solution in 50 mm citrate buffer at
pH 5.0 were made as the current was recorded as a function of
time.
Coin-Cell Battery Characterization
The previously described biocathodes and bioanodes were assem-
bled and sealed in a coin-cell casing to form a biobattery. Filter
paper was added between the two electrodes as a separator to
avoid short circuiting of the cell. For the particular case in which
GOx-based bioanodes were used in the coin cell, the filter paper
was modified with a solution of HRP [1 mg mL 1 HRP diluted in
a TBAB-Nafion (50 % v/v, in water)] to prevent laccase deactivation
by the build up of H2O2 coming from the reaction between GOx
and its natural electron acceptor, O2.[20] Buffer solution was injected
into the battery by holes located on the cathode side. The open-
circuit voltage (OCV) was measured and allowed to reach steady
state. Slow scan polarization (1 mV s 1 from the measured open cir-
cuit potential to 1 mV) was used to obtain polarization and power
curves by monitoring current as a function of potential. As the fer-
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rocene in the Fc-C6-LPEI is originally in its reduced state, experi- 2.2. Half-Cell Bioanode Characterization: Carbon Material
ments were recorded after a second polarization of the biobattery Studies
from OCV to 5 mV to guarantee that the Fc-C6-LPEI was in its oxi-
dized state before characterization in the presence of fuel. The fuel
Bioelectrocatalysis of the bioanodes was tested under different
solution was flushed through the battery to allow the solution
conditions at 25 8C in 50 mm citrate buffer at pH 5.0. To in-
inside the casing to be constant between experiments (namely,
100 mm substrate). The OCV was allowed to stabilize until it crease the current at the electrodes, CNT dispersions were
reached a steady state, and linear scan voltammetry (LSV) was per- added to the hydrogel modification. Different CNT dispersion
formed in the presence of 100 mm fuel solution.

2. Results
2.1. Half-Cell Biocathode Characterization: Carbon Material
Studies
Two different electrode materials were used in this study to
compare the bioelectrocatalytic currents obtained from the
oxygen reduction reaction from laccase at An-MWCNTs. TP and
CF electrodes were modified on a single side with the same
amount of biocathode ink. Figure 1 depicts the bioelectrocata-
lytic current obtained at these electrodes immersed in 50 mm
citrate buffer, pH 4.5. The larger porosity (from 0.94 to
0.98)[21, 22] and greater thickness (3.18 mm) of the CF material
relative to the same values of the TP material (0.78 and
0.19 mm, specification sheet) provided a higher capacity load-
ing for incorporation of the bioink into the conductive materi-
al. Current densities were higher on the CF electrodes with
a twofold and 1.5-fold increase relative to those on the TP
electrodes in the presence of dissolved and saturated oxygen,
respectively (TP: 115.4  10.0 and 299.6  33.5 mA cm 2 for dis-
solved and saturated O2, respectively; CF: 242.1 15.1 and
458.6  44.4 mA cm 2 for dissolved and saturated O2, respective-
ly). To estimate the benefit of the CF material on the bioink ca-
pacity loading at the electrode, the biocathode ink was depos-
ited on both sides of the CF material and the volume used
was increased by a factor of two and four on each side for
each electrode. Bioelectrocatalysis of oxygen reduction was
performed in quiescent solution (dissolved O2) and under satu-
rated oxygen conditions. All the current densities are reported
in Table 1. The resulting currents were increased two- and
threefold relative to those of the single-side-modified CF
electrodes.
Finally, both working conditions and stability experiments Figure 1. Representative cyclic voltammograms of laccase/An-MWCNT im-
were performed at pH 5.0 to assess the electrocatalytic current mobilized on TP electrodes (top) and CF electrodes (bottom) soaked in
50 mm citrate buffer at pH 4.5 in dissolved O2 (c) or under pure O2 bub-
that could be obtained in the biofuel cell experiment running bling (a) conditions recorded at 1 mV s 1.
under the same conditions. Upon first testing by CV, the cur-
rent recorded from An-MWCNT/
laccase biocathodes at + 300 mV
versus SCE was 682.3 
Table 1. Comparison of the catalytic current of different laccase/An-MWCNT-modified CF electrodes depending
66.3 mA cm 2. The current was on the bioink loading and oxygen concentration.[a]
monitored continuously by CV
and amperometric studies for Conditions Current density [mA cm 2]
Single side modification Two side modification
a period of 7 days. As shown in
Twofold increase in volume Fourfold increase in volume
Figure 2, electrocatalytic currents
of the biocathodes decreased dissolved O2 254.5  13.6 546.9  32.1 (2.3) 774.4  43.7 (3.0)
saturated O2 518.8  54.7 1180.0  110.3 (2.3) 1830.0  78.5 (3.5)
progressively to reach 65 % of
the original currents after 7 days [a] Cyclic voltammograms were recorded at 1 mV s 1 in 50 mm citrate buffer, pH 4.5. Current densities were
taken at 300 mV vs. SCE.
of continuous operation.

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Figure 2. Stability over time of laccase/An-MWCNT CF biocathodes. Current
recorded from CV experiments at E = 300 mV versus SCE (&) and from poten-
tiostatic experiments after 23 h of continuous polarization at E = 300 mV
versus SCE (&).
concentrations were assayed (0, 1, and 2 mg mL 1 CNTs in de-
ionized water). Figure 3 shows calibration curves of GOx-based
bioanodes modified with a Fc-C6-LPEI redox hydrogel on TP
electrodes. As expected, the presence of CNTs within the redox
hydrogel greatly enhanced the catalytic current at the bioe-
lectrodes upon the addition of glucose into the electrolyte.[23]
With a CNTs dispersion of 1 mg mL 1, the maximum current
density (Jmax) reached a plateau at around 100 mm glucose
(380.5  35.0 mA cm 2). No change was obtained upon replac-
ing the TP electrode by a CF-based bioanode (378.1 
33.5 mA cm 2 at 100 mm glucose). However, the thickness of
the CF allowed a larger quantity of hydrogel/enzyme mixture
Figure 3. Calibration curves obtained for GOx/Fc-C6-LPEI immobilized on TP
electrodes without the addition of CNTs within the redox hydrogel (~), with
the addition of a dispersion of 1 mg mL 1 CNTs (&) and 2 mg mL 1 CNTs (&)
upon successive additions of glucose in 50 mm citrate, pH 5.0 at 25 8C.
Epoised = Epa + 50 mV.
 2014 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
www.chemelectrochem.org
to be immobilized onto the electrodes. Twice the volume im-
mobilized led to a twofold increase in catalytic current at the
anodes (745.1  59.7 mA cm 2 at 100 mm glucose). Similar ex-
periments were performed on MWCNT/FDH-based CF bioe-
lectrodes made with a 1 mg mL 1 CNT dispersion. Amperomet-
ric measurements in the presence of 100 mm fructose resulted
in electrocatalytic currents of 40.6  7.5 mA cm 2, as shown in
Figure 4.
Figure 4. Calibration curves obtained for FDH/Fc-C6-LPEI immobilized on CF
electrodes with addition of a dispersion of 1 mg mL 1 CNTs upon successive
additions of fructose in 50 mm citrate, pH 5.0 at 25 8C. Epoised = Epa + 50 mV.
2.3. Coin-Cell Biobattery Design
Coin-cell biobatteries were assembled with CF-based biocath-
odes and CF-based bioanodes by using a 50 mm citrate buffer.
Polarization was performed to fully oxidize the redox hydrogel.
Upon OCV stabilization, a second polarization of the battery
was performed to assess the characteristics of the coin cell in
the absence of substrate. Finally, a solution of 100 mm fuel so-
lution was flushed into the coin cell. The OCV increased gradu-
ally as the amount of ferrocene was reduced by the enzymatic
reaction in the presence of the substrate. Figure 5 displays the
polarization curves for glucose and fructose coin cells in the
presence of 100 mm fuel solution at pH 5.0. The maximum cur-
rent densities were 31.3  3.0, 120.2  9.7, and 281.8 
3.7 mA cm 2 and the power densities reached 12.7  0.1, 29.9 
3.2, and 51.2  1.6 mW cm 2 in buffer, 100 mm fructose, and
100 mm glucose, respectively. Whereas the OCVs for both bio-
fuel cells in the presence of substrates were close due to the
use of the same mediator, currents were higher for GOx-based
biobatteries, as expected from the amperometric experiments
shown earlier. The glucose biobattery presented a typical po-
larization curve with the three limitations usually observed (ac-
tivation, ohmic, and concentration losses). On the other hand,
the fructose biobattery presented a current density peak that
should correspond to a diffusion limitation due to a decrease
in the local redox site concentration, as well as instability of
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Figure 5. Polarization (left) and power (right) curves obtained for laccase/
GOx or laccase/FDH coin-cell biobatteries in the absence or presence of sub-
strate at 1 mV s 1. All the electrodes were made with CF. Electrolyte: 50 mm
citrate, pH 5.0 at 25 8C.
the biobattery at high current densities. These results are in
agreement with the previous results obtained from the CV ex-
periments we reported for the two enzymes by using a FcMe4-
C3-LPEI.[24] The performances obtained were not as high as
those of other biobattery designs found in the literature, but
they could be improved by incorporating a redox polymer
with a lower oxidation potential or by optimizing the bioca-
thode ink and bioanode hydrogel loading. Furthermore, to the
authors’ best knowledge, this is the first example in which
a biobattery combines two bioelectrodes. Other biobattery de-
signs involve the use of hybrid technology by combining an
enzymatic bioelectrode and an abiotic electrode. The Minteer
group reported several biobattery designs based on nicotin-
amide adenine dinucleotide-dependent dehydrogenase bioan-
odes and Prussian Blue cathodes.[25–27] Another device propos-
es the use of the iodide/triiodide redox couple at the cathode,
whereas glucose was oxidized at a poly(methylene blue)/glu-
cose dehydrogenase bioanode.[28] Zhang’s group recently re-
ported a maltodextrin-based biobattery based on a vitamin K3
based bioanode (VK3 : E0 = 0.148 V vs. SCE[29]) and a Pt-based
cathode.[6] Also, there are a few examples in which the abiotic
electrode is the anode and the enzymatic electrode is the cath-
ode. In these cases, a zinc electrode is combined with a lac-
 2014 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
www.chemelectrochem.org
case-engineered biocathode. The OCVs of these biobatteries
are around 1.5 V, owing to the very low redox potential of Zn.
Their current and power densities are typically in the range
from a few mA cm 2 to mW cm 2. However, most of the current
gathered at the cathode can be attributed to O2 reduction on
the carbon material directly instead of being part of the lac-
case reduction process.[16, 30, 31] Moreover, electrode materials
can be further improved, as shown for the mesoporous materi-
al developed by Kano and co-workers to obtain efficient direct
electron transfer of FDH.[9] Nevertheless, performances ob-
tained in our coin-cell batteries are obtained by using only
200 mL fuel solution and transitions biobattery designs into
a traditional coin-cell design that is used commercially for reg-
ular self-contained batteries (i.e. lithium-ion batteries).
3. Conclusions
The use of CF electrodes allows a larger quantity of bioelectro-
catalyst to be immobilized at an electrode relative to that al-
lowed by conventional TP. These CF electrodes can be sealed
in a coin-cell casing design to form a biobattery. By using lac-
case at the biocathode and fructose dehydrogenase or glucose
oxidase at the anode, we were able to demonstrate the proof
of concept of this design working with a relatively small
volume of fuel solution. Upon combining a bioanode and a bio-
cathode into a biobattery, there are many new issues that
need to be addressed from this new design, such as the small
volume required and the production of hydrogen peroxide
within the battery. Further experiments will be performed to
increase the open-circuit voltage of the battery, which drasti-
cally limits the performances of the devices. Nonetheless, we
have shown that commercial battery casings are suitable to
characterize the performances of two different biobatteries,
and this could be the starting point for a more general stand-
ardization testing procedure for all the biobatteries in
development.
Acknowledgements
The authors would like to acknowledge the National Science
Foundation (NSF) (Grant no. 1057597) for funding. The authors
would also like to acknowledge the NSF CBET 0967988 program
for funding.
Keywords: biobatteries · biofuel cells · carbohydrates ·
conducting materials · enzymes
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Published online on August 11, 2014
ChemElectroChem 2014, 1, 1880 – 1885 1885