Bioresource Technology 102 (2011) 381–387

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Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Butler–Volmer–Monod model for describing bio-anode polarization curves

Hubertus V.M. Hamelers a,*, Annemiek ter Heijne a,b, Nienke Stein a,b, René A. Rozendal c,
Cees J.N. Buisman a,b
a
Sub-Department of Environmental Technology, Wageningen University, Bomenweg 2, P.O. Box 8129, 6700 EV Wageningen, The Netherlands
b
Wetsus, Centre of Excellence for Sustainable Water Technology, Agora 1, P.O. Box 1113, 8900 CC Leeuwarden, The Netherlands
c
Advanced Water Management Centre, The University of Queensland, St. Lucia, QLD 4072, Australia

a r t i c l e i n f o a b s t r a c t

Article history: A kinetic model of the bio-anode was developed based on a simple representation of the underlying bio-
Received 31 March 2010 chemical conversions as described by enzyme kinetics, and electron transfer reactions as described by the
Received in revised form 22 June 2010 Butler–Volmer electron transfer kinetics. This Butler–Volmer–Monod model was well able to describe the
Accepted 25 June 2010
measured bio-anode polarization curves. The Butler–Volmer–Monod model was compared to the
Available online 23 July 2010
Nernst–Monod model described the experimental data significantly better. The Butler–Volmer–Monod
model has the Nernst–Monod model as its full electrochemically reversible limit. Contrary to the
Keywords:
Nernst–Monod model, the Butler–Volmer–Monod model predicts zero current at equilibrium potential.
Bioelectrochemical system
Microbial Fuel Cell
Besides, the Butler–Volmer–Monod model predicts that the apparent Monod constant is dependent on
Anode anode potential, which was supported by experimental results.
Butler–Volmer Ó 2010 Elsevier Ltd. All rights reserved.
Monod

1. Introduction
Bioelectrochemical systems (BESs), such as Microbial Fuel Cells
(MFCs) (Logan et al., 2006; Rabaey and Verstraete, 2005) and
Microbial Electrolysis Cells (MECs) (Logan et al., 2008) use electro-
chemically active microorganisms on a bio-anode for the conver-
sion of chemical energy of organic materials directly into
electrical energy. BESs are constructed by electrically coupling a
bio-anode with a suitable cathode in an electrochemical cell.
The working principle of bio-anodes is based on the catalytic ac-
tion of electrochemically active microorganisms that grow on the
anode surface. The anode itself is chemically inert and serves as
a current collector and support for the electrochemically active
microorganisms. The electrochemically active microorganisms
convert organic material to carbon dioxide, protons, and electrons
and subsequently transfer the produced electrons to the anode sur-
face. The conversion of the organic material into carbon dioxide,
protons and electrons occurs inside the microorganism and the
conversion rate is determined by enzyme kinetics. The transfer of
electrons from the microorganism to the electrode however, occurs
at the interface between the microorganisms and the electrode
surface, and is described by electron transfer kinetics, like the But-
ler–Volmer relationship.
* Corresponding author. Tel.: +31 317 483447.
E-mail address: Bert.Hamelers@wur.nl (H.V.M. Hamelers).
In theory, the Gibbs free energy that is released in the oxidation
of organic material can be fully converted into electrical energy of
electrons. The efficiency of this conversion however, is typically
lower than 100% due to losses at the bio-anode. To quantify these
anode losses it is common practice to record the anode polarization
curve (Logan et al., 2006; Ter Heijne et al., 2008; Aelterman et al.,
2008; Manohar et al., 2008). Anode polarization curves show cur-
rent density as a function of the anode potential or vice versa
and, therefore, give a direct measurement of the energy losses at
the anode at a certain current density.
Only few papers have been dealing with the kinetics of the bio-
anode (Picioreanu et al., 2007, 2008; Marcus et al., 2007; Torres
et al., 2008). There is only a single model, the Nernst-Monod model
(Marcus et al., 2007; Torres et al., 2008; Finkelstein et al., 2006),
that specifically aims at modeling the bio-anode performance with
respect to the effect of substrate and anode potential. The Nernst-
Monod model is a modified version of the Monod model by consid-
ering the electrode as the final electron acceptor.
In this study, we will further explore the kinetics by developing
a kinetic model based on a simple representation of the underlying
biochemical conversions as described by enzyme kinetics, and
electron transfer reactions as described by the Butler–Volmer elec-
tron transfer kinetics. We will therefore refer to our model as the
Butler–Volmer–Monod model. This simple representation makes
it possible to derive an analytical solution of the Butler–Volmer–
Monod model. Such an analytical solution is attractive as it makes
description and analysis of polarization curves easier. We applied

0960-8524/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2010.06.156
382 H.V.M. Hamelers et al. / Bioresource Technology 102 (2011) 381–387
the Butler–Volmer–Monod model to a set of polarization curves
obtained under different growth conditions and anode materials.
The similarities and differences between the Butler–Volmer–
Monod model and the Nernst–Monod model are investigated and
discussed.
2. Model description
At the bio-anode, electrochemically active bacteria are capable
of oxidizing organic matter and transferring the electrons to the
anode. It is generally accepted that the first step is the biochemical
oxidation of the electron donor to CO2, protons and electrons,
transferred to a certain redox component, for example NAD+. The
second step, the transfer of electrons from NADH type redox com-
ponents to the anode is still an active area of research. Three dis-
tinct mechanisms for transfer from the redox component to the
anode have been proposed (Torres et al., 2010): direct contact, sol-
uble mediators, and a conductive matrix. In all mechanisms, heter-
ogeneous electron transfer is involved, which is brought about by a
redox component that is oxidized at the anode and transfers its
electron(s). In the direct mechanism, this redox component resides
at the outer cell surface, in the mediator mechanism this redox
component is a small soluble molecule that shuttles between the
cell and the anode. The nature of the conductivity of a conductive
solid matrix has not yet been revealed, it is however hypothesized
that bound cytochromes, i.e. redox components, play a role. These
mechanisms and their kinetic implications have been recently re-
viewed (Torres et al., 2010).
To develop a minimal model for bio-anode polarization curves,
we need to develop a kinetic description of microbial metabolism
that includes at least two processes: (i) biochemical oxidation of
a substrate, and (ii) heterogeneous electron transfer to the elec-
trode. The biochemical oxidation of the substrate occurs inside
the microorganism and yields the products and the released elec-
trons. The heterogeneous electron transfer occurs via a redox com-
ponent from the microorganism to the electrode surface (Fig. 1).
The model makes no explicit mechanistic assumption on the nat-
ure of the electron transfer from NADH to the final redox compo-
nent transferring the electron to the anode. It is assumed that
the biochemistry or the electron transfer, or a combination of both
processes is rate limiting. The effect of intermediate processes is
assumed to be that small that it does not significantly influence
the rate.
Anode Bulk
Microorganism
P P
Xox
e Xc
Xred
S S
Fig. 1. Kinetic scheme of the bio-anode. Substrate (S) from the bulk phase diffuses
to inside the cell and is converted by an enzymatic reaction to form the redox
component complex XC in the micro-organism. This is a biochemical conversion
into products (P) that diffuse to the bulk phase again. The electrons that are released
in the conversion are transported to the electrode via a redox component (Xox/Xred).
In our minimal model, the redox component that acts as the
electron acceptor in the biochemical oxidation reaction is assumed
to be the same redox component that acts as the electron donor in
the heterogeneous electron transfer to the electrode.
Accordingly, we describe the bio-anode as a three reaction sys-
tem. The first reaction is the reaction of the substrate (S) and the
oxidized redox component (Xox) to form a redox component com-
plex (XC) via an enzymatic reaction.
k1
S þ X ox ¢ X C
k2
This reaction is described by the normal mass action rate law
and has two constants describing the rate, the forward rate con-
stant k1 and the backward rate constant k2. The redox component
complex undergoes a second reaction upon which the products (P)
are formed together with the reduced redox component (Xred):
k3
X C ¢ P þ X red
k4
This reaction is characterized by the forward rate constant k3 and
the backward rate constant k4.
In the third reaction, the reduced redox component is oxidized
at the electrode while the electron is transferred:
k5
X red ¢ X ox þ e
k6
This latter reaction is the actual heterogeneous electron trans-
fer. This type of reaction has the specific characteristic that the
reaction rate is influenced by the electrode potential, both the for-
ward rate constant k5 and the backward rate constant k6 are thus a
function of the electrode potential.
The redox component connects all reactions and is the back-
bone of the process: the oxidized form is combined with the sub-
strate and becomes reduced via an intermediate complex, while
forming the products. The reduced form is re-oxidized upon liber-
ating the electron to the electrode. The transfer from electrons to
the redox component inside the microbial cell is considered to be
an enzyme-based reaction. We assume that the enzyme is present
in excess compared to the redox component.
The whole system can now be described as three mass balances
of the three different forms of the redox protein:
d
X ox ¼ k1  S  X ox þ k2  X C þ ðk5  X red  k6  X ox Þ ð1Þ
dt
d
X red ¼ k3  X C  k4  P  X red  ðk5  X red  k6  X ox Þ ð2Þ
dt
X C ¼ X T  X ox  X red ð3Þ
We assume that the total amount of the redox component is
constant inside the microbial cell and therefore the amount of re-
dox component complex can be described as the total amount of
redox component minus the oxidized and the reduced form of
the redox component (Eq. (3)).
A distinctive property of an electrochemical reaction is that the
rate constants of the heterogeneous electron transfer are depen-
dent on the electrode potential. The Butler–Volmer model is used
to describe this potential dependency. The Butler–Volmer model
is the standard model to describe electrochemical reactions and
has been shown to be applicable to large class of redox proteins
(Armstrong et al., 1993). The electrochemical rate constants k5
and k6 are given by:
h 0
i
0
k5 ¼ k exp ð1  aÞf ðEA  E0X Þ ð4Þ
h  0
i
0
k6 ¼ k exp af EA  E0X ð5Þ
 H.V.M. Hamelers et al. / Bioresource Technology 102 (2011) 381–387 383

In which, k0, standard heterogeneous rate constant (cm/s); a, trans- 2.3. Limiting current density
0
fer coefficient (–); f ; RT F
(1/V); EA, anode potential (V); E0X , formal po-
tential of redox component (V).
The transfer coefficient has a value between 0 and 1, and is typ- Imax ¼ n  F  X T  k3 ð10Þ
ically around 0.5 (Bard and Faulkner, 2001). The parameter Imax describes the maximum current density that
The primary output is the measured current density (I) at the can be obtained and can also be called limiting current density.
anode. This observed current is the net result of two opposite reac- This limiting current density is determined by the enzymatic reac-
tions occurring simultaneously at the anode surface: the oxidation tion, because the rate of the electrochemical reaction can be in-
of Xred giving rise to a forward anodic current density creased at will by increasing the anode potential.
If ¼ n  F  k5  X red , and the reduction of Xox giving rise to a back-
ward cathodic current density Ib ¼ n  F  k6  X ox . The observed cur- 2.4. Exchange current density
rent density at the anode is thus given by the difference between
the forward and backward current: The exchange current density is a measure of the maximum
I ¼ n  Fðk5  X red  k6  X ox Þ ð6Þ anodic current density that can be achieved at equilibrium condi-
tion, i.e. at zero current. At equilibrium, the resulting current den-
where, n, moles of electrons involved in the reaction; F, Faraday sity is zero, because the anodic current is compensated by an
constant (C/mol). equally sized cathodic current. The exchange current density is a
By substituting Eqs. (4) and (5) in (6), we find the more familiar measure for the reversibility of the reaction, and thus how fast
Butler–Volmer rate equation (Bard and Faulkner, 2001) for hetero- the electrochemical reaction of the redox component runs. It can
geneous electron transfer: be described by:
h  0 i
0
I ¼nF Iex ¼ n  F  X T  k  exp ð1  aÞ  f  E0X  ES=P ð11Þ
 h  0
i h  0
i
0
 k X red  exp ð1  aÞf EA  E0X  X ox  exp af EA  E0X
where ES/P, thermodynamical anode potential (V), which is the the-
ð7Þ oretical anode potential as calculated using the Nernst equation as
described in (Hamelers et al., 2010).
As the amount of any redox component X is expressed as its cov-
Combining Eq. (1)–(11) yields the Butler–Volmer–Monod mod-
erage (mol/m2), the current is expressed as current density. The sub-
el, being a steady-state solution for the current density as a func-
strate and products are expressed as concentrations (mol/m3).
tion of overpotential:
A comparable kinetic description has been used in the field of
voltammetry of electroactive enzymes, see for an overview Heer- 1  ef g
I ¼ Imax   ð12Þ
ing et al. (1998). Although conventionally, k4 is assumed zero, here K1  eð1aÞf g þ K 2 ef g þ KSM þ 1
we include k4 to assure that also the thermodynamic equilibrium
can be modeled. This equation contains the overpotential g, defined as EA  ES/P,
Substituting Eq. (3) in Eqs. (1) and (2) gives two differential and two lumped parameters: K1 and K2. These new parameters are
equations for Xox and Xred. When there is a steady-state situation, defined as:
the derivative terms are zero and S, P and the potential remain con-    0 
Imax k4
stant. For such a linear system a steady-state solution for Xox and K1 ¼ 1 þ P  þ exp f  E0X  ES=P ð13Þ
Iex k3
Xred can be straightforwardly found using matrix inversion. We
found the solution using MathCad routines. Substituting this solu-  
k3 KP
tion for Xox and Xred in the output equation for the current density K2 ¼ 1þ ð14Þ
k2 P
(Eq. (6)) yields a solution for the current density.
To make the model solution interpretable, we have rewritten It is important to note at this point that at steady-state, S and P
the model using more standard parameter representation (Cleland, are constant, and thus so is the equilibrium potential. This means
1963). Therefore, the following parameters have been introduced: that during recording of a polarization curve the values of K1 and
K2 remain constant, and that no individual kinetic constant can
2.1. Substrate affinity constant be determined from a polarization curve. The interpretation of
the parameters K1 and K2 will be discussed in Section 4.2.
k2 þ k3
KM ¼ ð8Þ
k1 3. Methods
The substrate affinity constant or the so-called Michaelis–Men-
ten constant describes the effect of substrate on the biochemical 3.1. Experimental
conversion. This constant is empirically determined as the concen-
tration at which half of the turnover is achieved. 3.1.1. Polarization curves
Polarization curves used for parameter fitting were obtained in
previous study (Ter Heijne et al., 2008). The setup consisted of four
2.2. Product inhibition constant
MFCs which were hydraulically connected in series and which con-
tained four different anode materials: flat graphite, roughened
k2 þ k3
KP ¼ ð9Þ graphite, Pt-coated titanium, and uncoated titanium. The data of
k4
the uncoated titanium anode were left out because of its bad per-
The product inhibition constant describes the extent to which formance. The anode was continuously fed with 20 mM KCH3COO
a certain product concentration leads to an inhibition of the turn- and 20 mM phosphate buffer at pH 7, and the catholyte was a
over rate. Although the inhibition constant looks similar to the 50 mM Fe(III)[CN]6 solution. pH was controlled at pH 7. The acetate
substrate affinity constant, it can in most cases not be interpreted concentration was high enough to avoid mass transfer limitations
similarly as the concentration at which half of the turnover rate is (Ter Heijne et al., 2008). Because of the pH control, buffer concen-
achieved. tration, continuous feeding, and the large volume to area ratio of
384 H.V.M. Hamelers et al. / Bioresource Technology 102 (2011) 381–387

the reactors, the concentrations of substrates and products can be ðRSSNM  RSSBVM Þ=2
F 2Nobs -4 ¼ ð15Þ
considered to be in steady-state and constant during the recording RSSBVM =ðNobs  4Þ
of the polarization curve.
The 4 denotes the number of parameters of the Butler–Volmer–
For each type of electrode material, the cells were subsequently
Monod model and 2 is the extra number of parameters of the But-
operated with different external loads. The effect of a load is that
ler–Volmer–Monod model compared to the Nernst–Monod model.
the cell operates at a certain anode potential. Each cell operated
An F-value of 0 would indicate that the Butler–Volmer–Monod
5–8 days at a specific load. The average anode potential during
model would add nothing to the description compared to the
the day proceeding the recording of a polarization curve was
Nernst–Monod model, while an F-value of 1 indicates that the
reported.
improvement is of the same order as the residual variance. An F-
Bio-anode polarization curves were obtained by dc-voltamme-
value >1 is needed to show that the improvement of the Butler–
try, using chronoamperometry with a potentiostat (Ivium Technol-
Volmer–Monod model compared to the Nernst–Monod model is
ogies, Eindhoven, The Netherlands). The cell voltage was decreased
significant. The significance level was calculated using the F-distri-
stepwise and was kept at each voltage during 120 s in order to let
bution. In this way it is assured that the additional parameters con-
the current stabilize. The measured range was a cell voltage of
tribute significantly to the description of the polarization curve.
0.65 V down to 0.30 V, decreased in steps of 0.050 V, until a stable
current was reached. When a maximum in the current density was
found, the measurement was terminated to prevent damage to the 4. Results and discussion
microorganisms. Anode potential was measured and collected
every 30 s during these measurements on a PC via a Fieldpoint 4.1. The Butler–Volmer–Monod model describes polarization curves
FP-AI-110 module (National Instruments, Austin, Texas). The last well
data point was selected for data presentation. During the last
30 s of these measurements, the current changed with less than Twelve different curves were fitted that were obtained from
0.5% for all three materials (Ter Heijne et al., 2008), so a steady- three different types of anodes that had been operated at different
state situation can be assumed. current densities and consequently different anode potentials. All
curves were fitted to both the Nernst–Monod and Butler–
Volmer–Monod model. Two typical examples illustrating the fit
3.1.2. Effect of acetate concentration of both models to the experimental data are shown in Fig. 2.
In addition, we studied the effect of acetate concentration and
anode potential on current density. This was studied in the same
cell containing a rough graphite anode. Potassium acetate, buffer
(25 mM) and nutrients were fed continuously at such rate that
HRT was 5 h. Acetate was fed at six different concentrations: from
20 mM down to 10, 5, 2, 1, and 0.5 mM. Each substrate concentra-
tion was tested for 2 days to obtain a steady-state situation. Anode
potential was first controlled at 0.4 V vs. Ag/AgCl, using a poten-
tiostat (Ivium Technologies, Eindhoven, The Netherlands). After all
acetate concentrations were tested, anode potential was controlled
at 0.3 V vs. Ag/AgCl and the same procedure was repeated. For
each acetate concentration, after 15 h, generally a stable current
density was found, deviating <5%. Average current density was
determined after 15 h of operation till the end of the experiment.
Acetate concentrations were determined using a Gas Chromato-
graph (GC). The GC (HP 5890 series II, Agilent Technologies,
Amstelveen, The Netherlands) was equipped with an AT-Aqua-
wax-DA column (Alltech) and a flame ionization detector (FID).
Temperature was raised from 80 to 210 °C, with 25 °C/min. Nitro-
gen was used as carrier gas.

3.2. Fitting the model to the experimental data

A residual is the difference between the measurement and the

predicted value for this measurement. The parameters were found
by minimizing the residual sum of squares (RSS) of the residuals.
As both the Butler–Volmer–Monod model and the Nernst–Monod
model are non-linear, minimization was done using non-linear
least-squares estimation. Minimization was performed using the
quasi-Newton as implemented in MathCad. As the Butler–Vol-
mer–Monod model has more parameters than the Nernst–Monod
model it is expected that the RSS of the Butler–Volmer–Monod
model (RSSBVM) is smaller than that of the Nernst–Monod model
(RSSNM). To test whether the RSSBVM was significantly lower, the
F-statistic was used. The F-statistic compares the improvement in
the description of the data (=(RSSBVM  RSSNM)/(additional parame- Fig. 2. Experimental data for the rough graphite anodes for dataset 3 (A) and 2 (B),
ters)) with the residual variance of the model Butler–Volmer– and the model fit for both the Butler–Volmer–Monod model and the Nernst–Monod
Monod model (=RSSBVM/(number of observations-4)). model. The Butler–Volmer–Monod model describes both datasets most accurately.
 H.V.M. Hamelers et al. / Bioresource Technology 102 (2011) 381–387 385

Table 1 redox protein electrochemistry, it was shown that a was in this

Parameters obtained from fitting of the experimental datasets to the Butler–Volmer– range: between 0.45 and 0.82 (Wang et al., 2005) and between
Monod model. RG, roughened graphite; Pt, Pt-coated titanium; FG, flat graphite.
0.42 and 0.46 (Hong et al., 2006).
Dataset Electrode Over Imax a K1 K2 F
potential (V)a (A/m2)
4.2. The Butler–Volmer–Monod model has the Nernst–Monod model
1 RG 0.08 4.865 0.489 6.7 15.4 17 as its full electrochemically reversible limit
2 RG 0.13 2.436 0.545 5.9 19.8 764
3 RG 0.07 3.009 0.5 1.2 24.2 2.4
4 RG 0.02 3.492 0.5 1.0 8.7 6.5 For some datasets (e.g. dataset 3 and 9 having an F-statistic of
5 Pt 0.07 4.323 0.477 7.2 17.1 19.1 2.4 and 1.9), both the Butler–Volmer–Monod and the Nernst–
6 Pt 0.12 2.117 0.536 5.6 22.1 154 Monod model describe the dataset nearly equally well. To investi-
7 Pt 0.06 2.826 0.5 2.1 25.6 6.8
gate the similarities and differences between the Butler–Volmer–
8 Pt 0.02 2.996 0.5 0.92 10.3 29
9 FG 0.08 3.001 0.5 2.4 26.8 1.9
Monod model and the Nernst–Monod model, we first rewrite the
10 FG 0.16 1.301 0.497 8.1 26.4 246 Butler–Volmer–Monod model in a form similar to the Nernst–
11 FG 0.08 2.929 0.5 1.8 16.3 19 Monod model. We can write the Butler–Volmer–Monod model as:
12 FG 0.03 2.996 0.5 0.92 10.3 29 !
 
a
Overpotential at which the anode had operated during the day before the
I 1  ef g S
¼ a g g
 KM
polarization curve was made. Imax K1  eð1 Þf  þ K2e f  þ1 þS
K 1 eð1aÞf g þK 2 ef g þ1

ð16Þ
Fig. 2A shows a dataset on which both models had a good fit. These while the Nernst–Monod model is written as follows (Marcus et al.,
data were obtained with the rough graphite anode operated at 2007):
0.43 V vs. Ag/AgCl during the day before the polarization curve   
was recorded (dataset 3 in Table 1). Fig. 2B shows a dataset on I 1 S
¼ ð17Þ
which the Butler–Volmer–Monod model had a better fit than the Imax 1 þ ef ðEEKA Þ KS þ S
Nernst–Monod model. These data were obtained with the same
where EKA = potential at which I = 1/2 Imax and KS the saturation con-
rough graphite anode operated at 0.37 V vs. Ag/AgCl during the
stant for a particular substrate.
day before the polarization curve was recorded (dataset 2 in
Both models have a similar structure consisting of two terms:
Table 1). In Fig. 2A and B we see that the Butler–Volmer–Monod
the first term describing the potential dependency of the current
model indeed predicts that the current density is zero at equilib-
density, and the second term being a Monod term describing the
rium, while the Nernst–Monod predicts a positive current density
substrate dependency. Comparing the Monod terms for substrate,
at equilibrium potential. The difference between both models is
we see that the Butler–Volmer–Monod term interprets the Monod
more clearly visible in Fig. 2B. This difference is a result of the fact
constant KA in the Nernst–Monod model as an apparent constant,
that the polarization curve is less steep, which is a situation that
consisting of the substrate affinity constant KM and a potential
cannot be handled by the Nernst–Monod model and which can
dependent term. At higher overpotential, the denominator with
be described by the Butler–Volmer–Monod model.
the potential term becomes 1 and the apparent constant KA equals
The details of the fit for each dataset is shown in Table 1. The
KM. This would suggest that the KM could be best estimated at high-
parameters Imax, a, K1, and K2 were obtained, and the residual
er overpotentials. This potential dependency of the apparent
sum of squares were calculated to determine the F-statistic. The
Monod constant is different from the Nernst–Monod model. Only
F-static compares the Butler–Volmer–Monod and the Nernst–
under certain conditions the models are more or less similar: when
Monod model. An F-statistic higher than one points to a better
K1 = 0 and overpotential is higher than 0.05 V.
description by the Butler–Volmer–Monod model compared to the
The main difference between the models occurs when K1  0.
Nernst–Monod model. Table 1 shows that the F-statistic is higher
We see this illustrated in Fig. 3.
than one in all cases. Thus, the Butler–Volmer–Monod model per-
Fig. 3 shows the Nernst–Monod model as the dashed black
forms better than the Nernst–Monod model in all cases. This was
line. The other lines are the Butler–Volmer–Monod model with
expected, as the Butler–Volmer–Monod model has more parame-
different K1 values. On the right, we see the dashed grey line with
ters than the Nernst–Monod model. To determine whether the
Butler–Volmer–Monod model is significantly better than the
Nernst–Monod model, the level of significance of the overall F-sta-
tistic describing all experiments was calculated; its value of 37.6
showed to be significant at the 99.99% level. This shows that over-
all the Butler–Volmer–Monod model gives a significantly better
description than the Nernst–Monod model. Furthermore, the extra
parameters are justified as the F-test takes into account that more
parameters lead to a better description.
Eq. (12) shows that when K1 is small, the exponential term con-
taining the transfer coefficient a has little effect on the polarization
curve. Consequently, it is impossible to estimate the value of a
accurately in cases K1 is small. In those cases (K1 < 3), a was set
at 0.5, as this is the value at which a can usually be approximated
(Bard and Faulkner, 2001). In the cases where K1 was >3 (5 data-
sets), it was possible to estimate an accurate value of a: the aver-
age was 0.51 with a standard deviation of 0.03. The fact that the
estimated a is near the expected value of 0.5 is an indication of
the suitability of the Butler–Volmer–Monod model. This expected
value of 0.5 for a holds not only for electrochemical reactions, Fig. 3. Effect of K1 on the polarization curves. K1 can be interpreted as the ratio
but also for bio-electrochemical reactions. For example, in direct between the biochemical reaction rate and the electrochemical reaction rate.
386 H.V.M. Hamelers et al. / Bioresource Technology 102 (2011) 381–387

K1 = 10. We see starting from this, that with decreasing K1 (grey

line and black line), the curve tends to shift towards the Nernst–
Monod model. We see that at K1 = 0 they coincide for overpoten-
tials >0.05 V. This means that if the electrochemical reaction is very
fast, both models approach each other.
Looking at the meaning of K1 we can get an understanding of a
more mechanistic interpretation within the framework of the But-
ler–Volmer–Monod model.
K1 is expressed as follows:
   0 
Imax k4
K1 ¼ 1 þ P  þ exp f  E0X  ES=P ð18Þ
Iex k3
We expect that the forward rate constant k3 is much higher than the
backward rate constant k4, as the microorganism needs to oxidize
the organic matter to obtain energy. Besides, the exponential term
will be small when the standard potential of the redox component
0
is higher than the anode equilibrium potential (E0X  ES=P > 0),
which is a prerequisite for electron
 transfer to occur. These assump-
 Fig. 4. Apparent KM is different for bio-anodes operated at different potentials.
0
tions imply that the term 1 þ P  kk43 þ expðf  ðE0X  ES=P ÞÞ ap-
proaches 1 and K 1  Imax
Iex
.
Fig. 4 shows the current density as a function of acetate concen-
K1 can thus be interpreted as the ratio on how fast the biochem-
tration for anode potentials of 0.4 and 0.3 V vs. Ag/AgCl. By fit-
ical reaction runs compared to the electrochemical reaction: the
ting the Monod equation to these curves, the apparent KM can be
limiting biochemical current density vs. the electrochemical ex-
determined. The apparent KM was 0.37 mM at 0.4 V vs. Ag/AgCl
change current density. When the electrochemical reaction is ex-
and 2.2 mM at 0.3 V vs. Ag/AgCl. So, experimentally we indeed
tremely fast, K1 will tend to zero and the Butler–Volmer–Monod
found a different apparent KM at different potentials. Such a poten-
model approaches the Nernst–Monod model. This makes sense,
tial dependency of the apparent Monod constant is predicted by
as an extremely fast electrochemical reaction is characterized by
the Butler–Volmer–Monod model and is not predicted by the
the fact that the Nernst equation is always valid at the electrode.
Nernst–Monod model. At high overpotential (Ean = 0.3 V vs. Ag/
In Table 1 we see that K1 ranges from 0.92 to 8.1, which shows that
AgCl), the exponential terms K 1 :eð1aÞf g and K 2 ef g approach zero
in general, the biochemical reaction is faster than the electrochem-
and the apparent KM approaches the true value for KM: 2.2 mM.
ical reaction.
We have developed the Butler–Volmer–Monod model based on
Under conditions of no product inhibition, it holds that KP  P.
general principles of biochemical and electrochemical kinetics. The
K2 can then be approached by:
  advantage is that insight can be gained in the occurring processes
k3 KP k3 and that additional relationships can be found, like the potential
K2 ¼ 1þ  ð19Þ
k2 P k2 dependency of the apparent Monod constant.

This means that K2 describes the ratio of the forward reaction

from redox component complex to product over the backward
reaction of the redox component complex to the substrate. We
would expect that the forward rate constant k3 is much higher than
the backward rate constant k2, because an organism needs to de-
grade the substrate to get energy and to survive. We therefore ex-
pect a K2 value to be appreciably bigger than one, which is indeed
the case (Table 1).
Although the parameters K1 and K2 are combinations of param-
eters describing more fundamental processes, a certain variability
is to be expected. An organism will adapt to different conditions,
which will be reflected in the parameter values. For example, a
microorganism will change its redox components in relation to
the anode potential to maximize the energy efficiency (Richter
et al., 2009). In this respect, it is interesting to note that a correla-
tion analysis revealed that at the 5% significance level, only the an-
ode potential influences the parameters K1 and K2. The type of
material showed to have no effect on K1 and K2.
4.3. The apparent Monod constant is potential dependent
The Butler–Volmer–Monod model predicts that the apparent
 
KM
Monod constant K eð1aÞf g þK ef g þ1
is dependent on anode poten-
1 2
5. Conclusions
A minimal model was developed that is suited for describing
and understanding bio-anode polarization curves with only three
parameters. This polarization model was developed from a combi-
nation of general enzyme kinetics and electrochemical kinetics and
is called the Butler–Volmer–Monod model. An analytical solution
was obtained. The polarization model was well able to describe
the measured bio-anode polarization curves. The Butler–Volmer–
Monod model was compared to the Nernst–Monod model, showed
a better description of the experimental data, and had the Nernst–
Monod model as its full electrochemically reversible limit. Further-
more, we showed that the Butler Volmer–Monod model predicts
zero current at equilibrium (zero overpotential) and that the
apparent Monod constant is dependent on anode potential as pre-
dicted by the Butler–Volmer–Monod model.
Acknowledgements
The authors thank Maarten Biesheuvel for his contribution to
the model development, Jingjing Zhao for her help with the exper-
iments, and Michel Saakes for his comments. Furthermore, we
thank César I. Torres for his critical and constructive review. This

tial, while the Nernst–Monod model assumes that the Monod con-
stant is independent on anode potential. The effect of potential on
apparent KM was determined in an experiment by flushing the cell
with different concentrations of substrate. Two anode potentials
were tested: 0.4 V vs. Ag/AgCl and 0.3 V vs. Ag/AgCl, each under
different substrate concentrations.
research was partly funded by SenterNovem, the Dutch govern-
mental agency for sustainability and innovation from the Ministry
of Economical Affairs; Besluit Energie Onderzoek Subsidie: Nieuw
Energie Onderzoek (grant No. NEOT01015), and supported by
Wetsus. Wetsus is funded by the Dutch Ministry of Economic Af-
fairs, the European Union European Regional Development Fund,
 H.V.M. Hamelers et al. / Bioresource Technology 102 (2011) 381–387
the Province of Fryslân, the city of Leeuwarden and by the EZ-
KOMPAS Program of the ‘‘Samenwerkingsverband Noord-
Nederland”.
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