DOI: 10.1002/cssc.
201100824
Flavins Secreted by Bacterial Cells of Shewanella Catalyze Cathodic Oxygen
Reduction
Huan Liu,[a, b] Shoichi Matsuda,[c] Kazuhito Hashimoto,*[b, c, d] and Shuji Nakanishi*[b, d]
Electric current is spontaneously generated whenever redox re-
actions are spatially separated on conductive substrates and
can lead to corrosion when both reactions proceed on a single
substrate. If corrosion is accelerated by metabolic activities of
microbes, such a phenomenon is called a microbiologically in-
fluenced corrosion (MIC).[1] MIC is recognized as an important
industrial issue because it causes serious damage to pipelines
and stainless-steel materials, particularly in sea-water, with
countermeasures requiring marked amounts of energy and
high costs.[2] In contrast to corrosion, redox reactions that
occur on two different substrates electrically wired through an
external load allow electric current to be harvested, represent-
ing the basis of microbial fuel cells (MFCs),[3.4] promising devi-
ces for acquiring electrical energy from aquatic sediments and
waste organic matter.
For both MIC and MFCs, extracellular electron transfer (EET)
between microbial biofilms and solid surfaces is a key process.
EET has been extensively studied in a few members of the bac-
terial genus Shewanella, as this process has broad application
in bioremediation, biogeochemical circulation, and bioelectrici-
ty.[5, 6] It is well-documented that EET to solid-state electron ac-
ceptors in these model species is mediated through the ex-
pression of abundant outer-membrane c-type cytochromes
(OMCs).[7] Interestingly, Shewanella cells can even transfer respi-
ratory electrons to solid-state acceptors at a distance through
secreted flavins that function as a shuttle between OMCs and
solids.[5a] Thus, respiratory electrons that are originally injected
into cells from organic matter can be either directly or indirect-
ly transferred to solids. Due to this property, studies of EET by
Shewanella cells have been mainly focused on bacterial anodic
[a] Dr. H. Liu
Key Laboratory of Bio-Inspired Smart Interfacial Science and
Technology of Ministry of Education
School of Chemistry and Environment
BeiHang University, Beijing 100191 (PR China)
[b] Dr. H. Liu, Prof. K. Hashimoto, Dr. S. Nakanishi
ERATO/JST
HASHIMOTO Light Energy Conversion Project
4-6-1 Komaba, Meguro-ku,Tokyo 153-8904(Japan)
Fax: (+ 81) 3-5452-5768
E-mail: hashimoto@light.t.u-tokyo.ac.jp
nakanishi@light.t.u-tokyo.ac.jp
[c] S. Matsuda, Prof. K. Hashimoto
Department of Applied Chemistry
The University of Tokyo
7-3-1 Hongo, Tokyo, 113-9656 (Japan)
[d] Prof. K. Hashimoto, Dr. S. Nakanishi
Research Centre of Advanced Science and Technology
The University of Tokyo
4-6-1 Komaba, Meguro-ku, Tokyo, 153-8904 (Japan)
Supporting Information for this article is available on the WWW under
http://dx.doi.org/10.1002/cssc.201100824.
1054  2012 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
reactions. Recently, there has been renewed interest in micro-
bial electrosynthesis to produce useful chemical materials,
which involves cathodic biocatalytic reactions in bio-electro-
chemical systems.[8] We report herein that the flavin com-
pounds secreted by cells of Shewanella loihica strain PV-4 cata-
lyze cathodic oxygen reduction (OR), which is a cathodic-coun-
ter reaction in both MIC and MFC systems.
Experiments were performed using a single-chamber, three-
electrode system[9] consisting of platinum wire and Ag/AgCl
(saturated KCl) as the counter and reference electrodes, respec-
tively, while a tin-doped In2O3 (ITO) glass substrate was used as
the working electrode. Prior to the electrochemical measure-
ments, a biofilm of PV-4 cells was formed on the ITO electrode
by electrochemically culturing the microbes at + 0.2 V in a de-
fined medium (DML) with lactate as the sole carbon source
and electron donor under anaerobic conditions, without any
agitation. After replacing the medium with fresh DML, the bio-
film-covered ITO electrode was poised at 0.5 V, where OR
could proceed for 2 days with continuous aeration of the
medium (see Experimental Section for details), and then cyclic
voltammetry (CV) measurements were taken.
Representative CV curves obtained at various conditions are
shown in Figures 1 a and b. Curve 1 in Figure 1 a is a CV ob-
tained for an ITO substrate in a deaerated DML medium lack-
ing microbes. A notable cathodic current did not flow until
0.6 V, the potential at which hydrogen evolution starts to
occur. Upon aeration of the DML solution, a small cathodic cur-
rent with an onset potential of 0.2 V began to flow (curve 2).
The cathodic current diminished when the DML solution was
deaerated by nitrogen gas bubbling, clearly indicating that OR
reactions were the origin of the cathodic current. A typical CV
obtained from a biofilm-covered ITO electrode in aerated DML
is shown in Figure 1 b (curve 3), in which an OR current with
the same onset potential as that on bare ITO was observed.
The cathodic current dramatically decreased after nitrogen
bubbling (curve 4, Supporting Information 1). The OR current
of the biofilm-covered ITO (curve 3) was larger than that of the
bare ITO (curve 2), which indicates that biofilms of strain PV-4
cells possess catalytic activity for cathodic OR, as was recently
reported by Freguia et al.[10] As the absolute value of the cur-
rent scattered in different batches of experiments, it has little
meaning to compare the curves quantitatively among the dif-
ferent batches. Therefore, we always performed control experi-
ments and evaluated the ratio of the currents in the absence
and presence of dissolved oxygen.
Notably, we detected a potential region (0.45 V to
0.55 V) where the absolute value of the cathodic current de-
creased with negative potential shift (curve 3). This anomalous
current density vs. potential relationship was observed even
when the potential was scanned in the positive direction. As
ChemSusChem 2012, 5, 1054 – 1058
 value of stationary current increases from about 1 mA and 6 mA
with negative shift of the applied potential from 0.35 V to
0.45 V, which indicates a long catalytic process on biofilm-
covered ITO. Further negative shift of the applied potential to
0.50 V, a potential within NFR region (point e in curve 3), de-
creases the stationary catalytic current a little, as suggested by
the corresponding CV (curve 3). The decrease of the stationary
current with negative shifts of the applied potential from
0.45 V (more positive than the NFR region) to 0.50 V
(within NFR region) is reproducible, which indicates the associ-
ation of NFR behavior with a long oxygen reduction process
more than with a change in redox condition.
Figure 2 shows the results of impedance analyses for the OR
reaction on ITO electrodes without (Figure 2 a) and with (Fig-
ure 2 b) an attached biofilm. The Cole–Cole plots taken at the
potentials indicated in Figure 1 a (points a–c) and Figure 1 b
(points d–f) are shown in Figure 2 a and b, respectively. Only

Figure 1. a) Cyclic voltammograms obtained for DML medium lacking mi-

crobes on bare ITO electrode under deaerated (curve 1) and aerated
(curve 2) condition in a same batch of experiments. b) Curve 3 and 4 are CV
curves obtained for DML medium on biofilm-covered ITO electrodes under
aerated and deaerated condition, respectively, in a same batch of experi-
ments. Curve 5 is the CV for filtrated supernatant on bare ITO electrode
under aerated condition. The scan rate is 10 mV s1. c) Current vs. time
curves for the biofilm-covered ITO at constant potentials of 0.35 V,
0.50 V, and 0.45 V under aerated conditions.

the absolute value of cathodic current generally increases with

negative potential shift (i.e., with increasing over-potential),
these results indicate that the cathodic OR mediated by strain
PV-4 cells exhibit a negative Faradaic resistance (NFR) charac-
teristic. As the negative control, both the cathodic currents on
bare ITO under aeration (curve 2) and on biofilm-covered ITO
under deaeration (curve 4) did not exhibit NFR behavior, fur-
ther suggesting that the biofilm of strain PV-4 possesses cata-
lytic activity for cathodic OR.
Figure 1 c shows the time course of cathodic currents on Figure 2. Cole–Cole plots obtained for a) DML medium on bare ITO elec-
trode, b) DML medium on biofilm-covered ITO electrode and c) DML
biofilm-covered ITO at constant potentials of 0.35 V, 0.5 V,
medium supplemented with 5 mm riboflavin on bare ITO electrode. Poised
and 0.45 V under aerated condition. The current is rather potentials are shown in the figure. The amplitude of the perturbations was
constant with time at each applied potential, and the absolute 10 mV. The frequency was scanned from 1 kHz to 1 mHz.

ChemSusChem 2012, 5, 1054 – 1058  2012 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim www.chemsuschem.org 1055
the plot obtained for the biofilm-covered ITO electrode at
point e, which is located on the negative slope in the CV, ex-
hibited a negative value in the real component of the impe-
dance spectrum, providing further evidence for the existence
of NFR. For the case of DML on bare ITO, the impedance spec-
trum displayed only positive values at potentials of 0.4 V,
0.5 V, and 0.6 V (Figure 2 a).
We confirmed that the filtered supernatant (the preparation
method is described in the Experimental Section) of the bacte-
rial cells suspension of DML electrolyte after electrochemical
measurement displayed a similar enhanced OR ability with NFR
property (Figure 1 b, curve 5) on bare ITO as that of the bio-
film-covered ITO. It should be noted that the onset potential
and magnitude of the cathodic current for the filtered super-
natant were nearly identical to those for the system with bio-
film (Figure 1 b, curve 3). These results suggest that the catalyt-
ic activity of the biofilm for OR is not related to bacterial respi-
ration or cell-surface enzymes such as OMCs, but to chemical
compounds secreted from the bacterial cells. Importantly, not
only Shewanella loihica PV-4, but also Shewanella oneidensis
MR-1 exhibit the identical behavior of biofilm-catalyzed OR.
Furthermore, as the NFR behavior can be obtained only when
both oxygen and the bacterial cells (or supernatant) exist in
the system (curve 3 and 5), it can be concluded that the differ-
Figure 3. a) Cyclic voltammograms for the DML supplemented with 5 mm ri-
ence in the current value between the positive (0.45 V) and
boflavin on bare ITO electrode under deaerated [dashed line, see (b) for
negative (0.55 V) end of the NFR potential region is at least a magnification] and aerated (solid line) conditions. The scan rate was
due to the contribution from biofilm (or supernatant). Based 10 mV s1. b) Magnification of the cyclic voltammogram in (a) under deaerat-
on curve 3, the current value at the 0.45 V and 0.55 V when ed conditions.
the potential was scanned in the positive direction is 7.5 mA
and 4.6 mA. Therefore, the contribution of catalytic effect of
the biofilm (or supernatant) reaches at least 2.9 mA, which cor- vins by Shewanella loihica strain PV-4 play a key role in the cat-
responds to 40 % of the current observed. From the repeated alytic activity of the as-formed biofilms for cathodic OR. The
experiments, we confirmed the contribution from the biofilm impedance spectrum for the OR reaction on bare ITO electrode
(or supernatant) ranges between 39 % and 54 %, which clearly with riboflavin gave a negative value (Figure 2 c) only at
demonstrated that the existence of the biofilm (or superna- 0.5 V, a potential located at negative slope in the CV
tant) can enhance the cathodic OR reaction. (Figure 3). Taken together, it directly evidences the involve-
What is the secreted compound that enhances the observed ment of flavins secreted by bacterial of Shewanella in cathodic
cathodic OR on biofilm-covered electrodes? As mentioned, OR.[8a, 10]
members of the genus Shewanella secrete flavins, which are Under deaerated conditions, in which no oxygen-reduction
capable of mediating long-distance EET to solid metal oxide current flows, only peaks assignable to the redox reactions of
acceptors.[5a] Here, we also detected flavin in the filtered super- riboflavin were observed for the DML supplemented with 5 mm
natant by fluorescence spectroscopy,[11] at a concentration of riboflavin on bare ITO electrode (Figure 3, dashed line). The
approximately 2 mm (Figure S1). It has also been demonstrated midpoint potential of the redox peak estimated from the CV
that synthetic quinone analogues, including flavins, adsorbed (Em  0.43 V) is close to the NFR potential, suggesting that
on a cathode have catalytic activity for OR reactions.[12, 13] the catalytic activity of riboflavin depends on the redox-state
Therefore, we speculated that the catalytic activity of the strain of riboflavin itself. Two electrons are transferred when the fully
PV-4 and MR-1 biofilms for the cathodic OR originated from se- reduced form of quinone (or quinone analogues) (Qred) is oxi-
creted flavins. Bond et al specified the flavin derivatives secret- dized to the fully oxidized form (Qox), or vice versa, via a semi-
ed by strain MR-1 as riboflavin and riboflavin-5’-phosphate.[5a] quinone one-electron transfer intermediate (Qsemi).[12, 13] Of these
To confirm our hypothesis, the CV for DML supplemented with three states of quinone, Qred and Qsemi can serve as the electron
5 mm riboflavin under aerated conditions (Figure 3, solid curve) transfer catalyst for cathodic reactions. As suggested by Tatsu-
on the ITO electrode was examined, which showed the identi- mi et al.,[12a] the redox potential of the Qsemi/Qox reaction is
cal onset potential for the OR reaction as that for the biofilm more negative than that of Qred/Qsemi in solutions of pH  7, in-
(curve 3) and filtered supernatant (curve 5). Notably, the CV dicating that O2 reduction by Qsemi is thermodynamically more
also exhibited NFR at an identical potential region (0.45 V to favorable than that by Qred. Actually, it has been confirmed
0.55 V) of that on biofilm-covered ITO under aeration (Fig- both by experimental data and theoretical simulation[12] that
ure 1 b, curve 3). These results clearly indicate that secreted fla- semi-quinone intermediates play a predominant role in qui-

1056 www.chemsuschem.org  2012 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim ChemSusChem 2012, 5, 1054 – 1058
none autoxidation, which can result in a reduction peak (i.e.,
a narrow potential region that gives maximum OR current) in
both positive- and negative-scan of the CV curve (i.e., the ap-
pearance of the NFR behavior) at a potential close to the mid-
point potential of adsorbed quinone. Based on this observa-
tion, the NFR property that appeared in the CV for the DML
supplemented with synthetic riboflavin on bare ITO electrode
can be explained as follows: Near the onset potential, most of
the adsorbed flavin compounds are in the Qox form and do not
possess catalytic activity for O2 reduction. With negative poten-
tial shift, the ratio (or electrode coverage) of Qsemi and Qred in-
creases, and the catalytic activity correspondingly increases.
However, if the electrode potential is shifted further negative,
most of the adsorbed flavins are in the Qred form, and the cov-
erage of Qsemi decreases.[12a] Thus, the catalytic activity of ad-
sorbed flavins exhibits a maximum at the potential region
where the coverage of Qsemi is the largest, resulting in the ap-
pearance of NFR. In electrochemical systems, Faradaic resist-
ance is generally positive, that is, the Faradaic current generally
increases with increasing over-potential. However, the Faradaic
resistance can be negative when: (a) the coverage of adsorbed
promoter decreases, (b) the coverage of adsorbed inhibitor in-
creases, or (c) the concentration of electroactive species de-
creases with increasing overpotential.[14] The NFR reported in
the present work can be classified as case (a), in which the pro-
motion effect of semi-quinone plays the key role.
In addition to flavins and quinones, OMCs play a crucial role
in mediating EET by Shewanella cells. Moreover, OMCs have
been detected dissociated from cells in biofilms and shed
membrane vesicles,[15] suggesting that these proteins are also
secreted extracellularly. Previously, Freguia et al.[10] concluded
that the catalytic activity for cathodic OR was attributable to
the OMCs located on living Shewanella putrefaciens cells and/
or present in the medium. This conclusion is supported by the
observation that the addition of hemin, a model heme mole-
cule, catalyzed the cathodic OR with a similar onset potential
to filtered supernatant lacking cells.[10] However, hemin and
heme-protein (such as c-type cytochromes) exhibit significant
different catalytic activity.[16] Furthermore, the addition of
hemin did not result in a detectable NFR (Figure S2). Therefore,
we conclude that the secreted molecules mainly catalyzing the
cathodic OR are not OMCs.
The present work demonstrates that secreted flavin com-
pounds by Shewanella species can catalyze cathodic OR. Nota-
bly, as flavins are diffusive species, they can catalyze cathodic
reactions at positions distant from the anodic reaction sites
where bacterial respiratory electron transfer occurs (i.e., an
anodic reaction proceeds). As Shewanella cells secrete flavin
compounds even under aerobic conditions and the onset po-
tential of the bacterially mediated anodic reaction ( 0.4 V)[6c]
is more negative than that of cathodic OR (ca. 0.2 V), natural
batteries can be formed around Shewanella biofilms, leading
to substrate corrosion (FigureS3). We anticipate that our find-
ings will provide new insight for developing methods to pre-
vent MIC and to improve MFC performance.
ChemSusChem 2012, 5, 1054 – 1058  2012 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
Experimental Section
Microbes preparation: Shewanella loihica PV-4 were cultured aer-
obically in 10 mL of marine broth (MB, 0 g L1) at 30 8C for 24 h.
Then, the cells were collected and washed three times with de-
fined media [DML: NaHCO3 (2.5 g), CaCl2·2 H2O (0.08 g), NH4Cl
(1.0 g), MgCl2·6 H2O (0.2 g), NaCl (10 g), and HEPES (7.2 g) per liter
with lactate (10 mm L1) as carbon source, pH 7.8], and finally re-
suspended into fresh DML for further aerobic cultivation at 30 8C
for 24 h using lactate as a carbon source. In order to form thick bi-
ofilms on the ITO electrode, high concentrations of the cell suspen-
sion in the electrochemical cell were used in these experiments,
with an optical density at 600 nm of 2.0.
Electrochemical measurements: A single-chamber, three-elec-
trode system was used to monitor the electrochemical behavior of
the microbes. An Ag j AgCl (sat. KCl) and a platinum wire were
used as reference and counter electrode, respectively. ITO glass
with the area of 3.14 cm2 was used as the working electrode. 4 mL
DML containing lactate (10 mm) was used as electrolyte. For deaer-
ated conditions, the electrochemical cell was deaerated by N2 bub-
bling for 30 min before measurements with a final dissolved O2
concentration of 0.1 ppm (Pre-Sens, Microx TX3 trace). The temper-
ature was kept at 30 8C in pH 7.8.
Prior to the electrochemical measurement, a biofilm of strain PV4
was formed on the ITO electrode by electrochemically culturing
the microbes at + 0.2 V in DML with lactate(10 mm L1) as the sole
carbon source and electron donor for 40 h under anaerobic condi-
tion without agitation. Then, after replacing the medium with fresh
DML, the biofilm-covered electrode was poised at a constant po-
tential where oxygen reduction could proceed (here, 0.5 V was
used) for 2 days with continuous air bubbling. Then, the cyclic vol-
tammogram was measured by using an automatic polarization
system (Compactstat, Ivium) with a scan rate of 10 mV s1.
Supernatant preparation: First, a biofilm of PV-4 cells was formed
on ITO by electrochemical culturing at + 0.2 V. Then, to remove
planktonic cells in the media, the supernatant in the electrochemi-
cal cell was carefully replaced with fresh DML medium by using
pipettes. After the replacement, the electrode potential was kept
constant at 0.5 V, at which the O2 reduction reaction proceeded
for two more days with air bubbling. Then the whole solution was
collected and centrifuged in order to remove the majority of the
cells in the solution. The remaining cells (average size of 0.6 ~ 1 
1.5 ~ 2 mm) were further removed using a filter with a pore diame-
ter of 0.2 mm (Toyo Roshi Kaisha Ltd., Japan). The resulting solution
was used as supernatant sample in the experiments.
Acknowledgements
This work was financially supported by Exploratory Research for
Advanced Technology (ERATO) program of the Japan Science and
Technology Agency (JST).
Keywords: biochemistry · electrochemistry · fuel cells ·
microbiology · redox chemistry
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Received: December 19, 2011
Published online on April 4, 2012
ChemSusChem 2012, 5, 1054 – 1058