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Microbial solar cells: applying

photosynthetic and electrochemically


active organisms
David P.B.T.B. Strik, Ruud A. Timmers, Marjolein Helder, Kirsten J.J. Steinbusch,
Hubertus V.M. Hamelers and Cees J.N. Buisman
Sub-Department of Environmental Technology, Wageningen University, Bomenweg 2, P.O. Box 8129, 6700 EV Wageningen,
The Netherlands
Microbial solar cells (MSCs) are recently developed tech-
nologies that utilize solar energy to produce electricity or
chemicals. MSCs use photoautotrophic microorganisms
or higher plants to harvest solar energy, and use elec-
trochemically active microorganisms in the bioelectro-
chemical system to generate electrical current. Here, we
review the principles and performance of various MSCs
in an effort to identify the most promising systems, as
well as the bottlenecks and potential solutions, for real-
life MSC applications. We present an outlook on future
applications based on the intrinsic advantages of MSCs,
specically highlighting how these living energy sys-
tems can facilitate the development of an electricity-
producing green roof.
Introduction
Society is facing local and global challenges to secure the
needs of people and planet [1,2]. One of those needs is
energy, which should be available in the form of electricity
or fuels, ideally produced from a renewable source via an
efcient and clean conversion process. Microbial solar cell
(MSC) is the collective name for new biotechnological
systems that integrate photosynthetic and electrochemi-
cally active organisms to generate in situ green electricity
or chemical compounds, such as hydrogen, methane, etha-
nol and hydrogen peroxide [35]. The MSC builds on the
discovery of electrochemically active bacteria and the sub-
sequent development of microbial fuel cells (MFCs) [68],
which typically clean wastewater and generate electricity
from biodegradable organic compounds present. Within
the MFC, electrochemically active bacteria at the anode
oxidize organic compounds and deliver electrons to the
anode. These electrons ow through a power harvester
to the cathode, where electrons are delivered to reduce
oxygen [9]. In an MSC, photosynthetic organisms use
sunlight to produce organic matter that is further con-
verted into electricity using the MFC [10,11]. The most-
investigated MSC is the plant MFC, which has a living
plant that delivers organic matter via its roots to electro-
chemically active bacteria in the MFC [10,1217].
Our aim is to review the principles and performance of
MSCs, and to describe the challenges and the outlook for
future applications of these technologies. Various MSCs
have been described recently and these can be categorized
according to the way solar energy is captured and the mode
of organic matter transfer from the photosynthetic portion
to the fuel cell. Both the reported and potential perform-
ance of different MSCs are analyzed to identify bottlenecks
and possible solutions. Currently, it is not possible to
predict the cost-effectiveness of the technology; however,
on the basis of known advantages of MSC technology,
potential applications and tradeoffs with other renewable
energy generation technologies are discussed.
Principles and performance of MSCs
The basic principles of MSCs, as illustrated in Figure 1,
are: (i) photosynthesis; (ii) transport of organic matter to
the anode compartment; (iii) anodic oxidation of organic
matter by electrochemically active bacteria; and (iv) ca-
thodic reduction of oxygen. We have categorized the MSCs
below according to the way in which solar energy is cap-
tured and the mode of organic matter transfer: a higher
plant with rhizodeposition; a phototrophic biolm with
diffusion; or a photobioreactor or coastal marine ecosys-
tem, which use pumps for translocation. The in-depth
bioelectrochemical principles of all systems are yet to be
fully revealed [3,7,1824]. Table 1 provides an overview of
recent developments in MSC performance and efciency.
Plant microbial fuel cell
MSCs with living higher plants are called plant microbial
fuel cells (PMFCs) [10]. In PMFCs, plant roots directly fuel
the electrochemically active bacteria at the anode by ex-
creting rhizodeposits [10,1217]. Rhizodeposition of plant
roots is the excretion of organic compounds into the soil,
including sugars, organic acids, polymeric carbohydrates,
enzymes and dead-cell material. The rhizodeposits account
for approximately 2040% of plant photosynthetic produc-
tivity, and these compounds can be degraded by a mixture
of microorganisms [23]. When the plant is growing with its
roots in the MFC, electricity is continuously generated in
situ. The rst published PMFC study estimated that net
power generation of 21 GJ ha
1
year
1
(67 mW/m
2
) is
theoretically possible under Western European (i.e. Neth-
erlands, Belgium and France) climate conditions (Box 1)
[10]. This net yield is similar to that for conventional
Review
Corresponding author: Hamelers, H.V.M. (bert.hamelers@wur.nl).
0167-7799/$ see front matter 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tibtech.2010.10.001 Trends in Biotechnology, January 2011, Vol. 29, No. 1 41
biomass electricity production systems, including digestion
of energy crops, which achieve net power generation of 2.8
70 GJ ha
1
year
1
(based on biogas production of 160400
GJ CH4 ha
1
year
1
[25], gas combustion efciency of 25%
[26] and energy input of 30% [27]), and biomass combus-
tion, which achieves net power generation of 2791 GJ
ha
1
year
1
(based on biomass productivity of 812 ton dry
weight ha
1
year
1
, a heating value of 1820 GJ/ton, bio-
mass combustion efciency of 2040% and energy input of
5%[28]). The theoretical PMFCpower output of 21 GJ ha
1
year
1
is a relatively conservative estimate, considering
that a multidisciplinary European research consortium
(www.plantpower.eu) has estimated that the power output
of the PMFC could reach 1000 GJ ha
1
year
1
(Box 1).
Three PMFC studies have integrated the anode into the
sediment in which plants were growing [12,13,16]. In these
studies, rhizodeposits fromplants and organic matter from
the sediment were available for current generation. Intro-
duction of growing rice plants in an MFC resulted in a
sevenfold increase in power output compared to the sedi-
ment MFC [12]. Outdoor experiments in Japan have also
been performed in a rice paddy eld [13,16]. However, in
these cases, power output was not higher than that
reported for a sediment MFC without plants [13,29].
The difference in power output between the rice paddy
and sediment MFC experiments might be the result of a
variety of factors, including the presence of rice plants, the
sediment composition, the microbial species and the fuel
cell design [30].
Of all MSCs reviewed, the Spartina anglica PMFC
study achieved the highest long-term current and power
density (PD) [14], with an average PDof 50 mW/m
2
over an
operating time of 33 days.
Microbial communities at the anode in PMFCs have
been analyzed to elucidate the principles and performance
of PMFCs. The most common bacteria are from the genus
Desulfobulbus or the Geobacteraceae [17], or were closely
related to Natronocella, Beijerinckiaceae, Rhizobiales or
Rhodobacter [13]. Some species, such as Geobacter sulfur-
reducens, are electrochemically active [31]. However, it has
not been shown whether electrochemically active species
are indeed present and active in a PMFC.
MSCs with phototrophic biolms
Solar energy is converted to electricity by growing a photo-
trophic biolm on the anode of a fuel cell (Table 1)
[11,19,3235]. MSCs with phototrophic biolms have a
self-organizing biolmcontaining Chlorophyta and/or Cya-
nophyta and canoperate for sustained periods of more than
20 days [34]. All studies to date have used mixed microbe
populations, which probably includes electrochemically
active bacteria. An exception is one study in which a pure
culture of Synechocystis PCC-6803 was applied to generate
an electrical current [19]. This cyanobacterium is able to
form electrically conductive nanowires when cultivated
under carbon dioxide limitation and excess light. Thus,
Synechocystis can be responsible for transfer of electrons
from the microorganism to the anode [19,36].
Some of the MSCs include sediment, which provides
additional organic matter. One study estimated that the
2.5-cm-thick marine sediment applied contained enough
organic matter to operate the system for 22 years [35]. To
date, the theoretical output for an MSCwith a phototrophic
biolm has not been estimated. Based on primary carbon
production of 250 g m
2
year
1
by benthic biolms in The
Netherlands, MFC energy recovery of 60% and glucose as
the carbon composite [37,38], we have estimated a maxi-
mum power output of 61 mW/m
2
[34,35]. This value is of
the same order of magnitude as for PMFCs [10]. The
maximumaverage PDfor MSCs with phototrophic biolms
was 7 mW/m
2
, which is sevenfold lower than for the best
PMFC [14] and 11% of the maximum PD estimated for
MSCs with phototrophic biolms (Table 1) [35].
MSCs with photobioreactors
MSCs can use photobioreactors to harvest solar energy via
photosynthetic microorganisms such as algae [19,3941].
Figure 2 shows an example of an MSC with a photobior-
eactor and an anaerobic digester. The digester pretreats
the photosynthetic metabolites and the microorganism
before supplying them to the MFC [40]. Photobioreactors
with algae can achieve photosynthetic active radiation
(PAR) (solar spectral range of 400700 nm, which can be
used by microalgae for photosynthesis) photosynthetic
efciencies of 15%. For MFC energy recovery of 29%, a

Membrane
(d) Cathode
O
2
CO
2
e
-
H
+
H
2
O O
2
CO
2
e
-
Photosynthetic
organisms
Electrochemically
active microorganisms
Electricity
(a)
(b) Organic matter
Sun
(c) Anode
TRENDS in Biotechnology
Figure 1. Model of a microbial solar cell including the basic principles. (a)
Photosynthesis (6CO
2
+6H
2
O!C
6
H
12
O
6
+6O
2
). (b) Transport of organic matter to the
anode compartment. (c) Anodic oxidation of organic matter by electrochemically
active bacteria (e.g. C
6
H
12
O
6
+12H
2
O!6HCO
3

+30H
+
+24e

). (d) Cathodic reduction


of oxygen to water (6O
2
+24H
+
+24e

!12H
2
O).
Review
Trends in Biotechnology January 2011, Vol. 29, No. 1
42
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Review Trends in Biotechnology January 2011, Vol. 29, No. 1
43
PD of 2806 mW/m
2
is theoretically possible under Western
European climate conditions [39,42].
The best results have been achieved with Chlorella in a
photobioreactor, for which a photosynthetic efciency of
6.3% (PAR-based) was reached. With a power conversion
efciency (PCE) of 0.04%, this system most effectively
converted light energy into electricity of all reviewed MSCs
(Table 1). This resulted in average PD of 14 mW/m
2
, which
is only 0.5% of the theoretical maximum [39]. It is impor-
tant to note that for the production of photosynthetic
metabolites in photobioreactors, energy of up to 10 W/m
2
is needed for mixing and removal of oxygen [39]. Thus, for
the current state of the art, MSCs with photobioreactors
yield no net electricity.
MSCs within a coastal marine ecosystem
MSCs can be integrated into a coastal marine ecosystem
[43]. Such ecosystems use solar energy and produce phy-
toplankton such as macro-algae and zooplankton that oat
in the ocean. If these substrates are harvested, electricity
can be generated by a MFC [41,43,44]. For real-life imple-
mentation, it was envisioned that pumps could be used to
feed raw seawater to a 40-km-long tubular MFC to gener-
ate electricity [43]. It has been estimated that MSCs in
coastal zones, which account for 10% of the ocean, can
generate electrical power of 2.416 TWh/year, which is
0.010.05 mW/m
2
when divided by the surface area
[43,45]. This PD is more than three orders of magnitude
lower than for MSCs that use higher plants or phototrophic
biolms. Thus, for the current state of the art, estimates of T
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Box 1. Electricity generation potential of PMFCs
The first estimate for realistic electricity production by a PMFC under
Western European conditions was 21 GJ ha
1
year
1
(67 mW/m
2
)
[10]. This estimate was based on: (i) average solar radiation of
150 W/m
2
in Western Europe (i.e. Netherlands, Belgium and France);
(ii) average photosynthetic efficiency of 2.5%; (iii) common rhizo-
deposition of 40%; (iv) rhizodeposit availability for microorganisms
of 30%; and (v) MFC energy recovery of 29%, including a growth
season of 6 months [10]. This potential was based on the
technological state of the art in 2008 using general data on the
conceptual process steps of the PMFC.
In 2010, a PMFC using S. anglica yielded long-term power
generation of 50 mW/m
2
[14]. If we extrapolateoof these results to
a 6-month growth season, 25 mW/m
2
could be produced on a yearly
basis, which accounts for 37% of the estimated maximum. At
present, a multidisciplinary European research consortium
(www.plantpower.eu) is working towards optimal electricity pro-
duction of 1000 GJ ha
1
year
1
(3.2 W/m
2
). This value is based on
the highest data reported for the conceptual process steps. With
average solar radiation of 150 MW/km
2
in Western Europe [80],
increased photosynthetic efficiency of 5% [22], a majority (70%) of
photosynthates transported to the soil [81] and possible 60% energy
recovery of these photosynthates by the MFC [38], power output of
3.2 W/m
2
would be possible. For application in natural conditions, it
is expected that 50% of this output (1.6 W/m
2
) could be harvested. Of
course, it is recognized that these values all depend on the system
constituents, the environmental conditions and the time course of
the experiment. Moreover, challenges mentioned in this review
have to be surmounted. Nevertheless, this example shows that
there is room for optimization to achieve higher power output. The
primary challenge is to further understand the principal processes of
PMFCs to subsequently design and operate PMFCs with higher
power outputs. When further knowledge is available, mechanistic
models can provide future estimates of power generation [82].
Review
Trends in Biotechnology January 2011, Vol. 29, No. 1
44
the energy input are 18 times more than the potential
electricity output [43].
Challenges in improving energy recovery
Reviews in the previous section of the most recent expecta-
tions for theoretical power generation and the performance
achieved reveal that PMFCs and phototrophic biolms
have the highest power generation (50 and 7 mW/m
2
,
respectively) [14,35] and highest estimated net power
potential (67 and 61 mW/m
2
, respectively). Thus, PMFCs
and phototrophic biolms are the most promising MSC
systems. Overall, MSCs are robust, with operating times in
the range 5175 days (Table 1) [12,34]. By contrast, other
MSCs use chemical catalysts, which poison the system
within hours and are thus not self-sustaining [4649].
MSCs with catalysts generate fuels such as hydrogen in
situ that are then oxidized via conventional fuel cells.
An important question is howthe PDcan be increased to
obtain a cost-effective MSC. This question cannot be an-
swered yet, because all MSCs developed to date are labo-
ratory-scale systems and are not designed for scale-up. In
addition, insufcient and incomplete data are available for
all major processes, which precludes accurate calculations.
For example, there are no measured data available on the
coulombic efciency (CE; fraction of electrons from the
totally oxidized electron donor that are transferred to
the anode) in MSCs. Determination of the exact carbon
and electron uxes, and therefore the CE, is experimental-
ly challenging at present.
However, MSCperformance may be improved inpursuit
of the estimated maximums, as there are many approaches
possible to increase the PD. There are many parameters
that determine the PD of MSCs. Some parameters are
comparable to those identied within the MFC research
eld and can be optimized using the same principles. For
example, fuel cell performance can be improved by lower-
ing the internal resistance (IR), which is between 10 and
1800 V (Table 1). In the following paragraphs, we review a
number of MSCstudies to highlight specic challenges and
opportunities for improving power output.
Increase substrate ux from photosynthetic to
electrochemically active organisms
It has been observed that MSCs, such as the PMFC, can be
substrate-limited [14], suggesting that the anode compart-
ment comprising electrochemically active bacteria can
oxidize more organic matter (i.e. electron donors) than
supplied. Thus, improving the substrate ux of easily
biodegradable exudates, for example via an increase in
rhizodeposition, will probably enhance the overall energy
recovery of the PMFC. The literature reveals several
mechanisms that enhance rhizodeposition [50,51]. The
choice of plant plays a major role in the quantity and
composition of rhizodeposits [23,52]. The MSCs in Table
1 have current densities that are considerably lower than
those of conventional MFCs, which achieve values up to 6.5
A/m
2
[38,53]. Although substrate ux does not solely de-
termine the current density, the values shown in Table 1
indicate that several MSCs could face substrate limitation.
Complex substrates can become more available to electro-
chemically active microorganisms via pretreatment (e.g.
hydrolysis) of complex electron donors [40,53]. In one study
using an anaerobic digester and an MFC, the algal sus-
pension was partly digested to methane and the remaining
substrate was fed to the anode of the MFC [40]. Applying a
hydrolysis stage rst instead of anaerobic digestion and
subsequent feeding to the MFC anode might make more
electron donors available for electrochemically active
microorganisms [40].
An improvement in substrate availability is also needed
to operate MSCs for prolonged periods at the maximum
PD. MFC power output can be increased by bringing the
external resistance close to the internal resistance of the
system[54,55]. However, this approach for the maximizing
power output is only effective when the substrate ux of
the systemis increased as well [54]. It has been shown that
an optimization strategy involving decreasing the external
resistance to match the internal resistance in a PMFC was
unsuccessful, possibly owing to substrate limitation
[14,15]. The same study showed that, based on maximum
compared to average PDs, a successful maximization strat-
egy could lead to a tenfold increase in power output [15].
Decrease the oxidation state of organic matter derived
from the photosynthetic organism
MSCs use a wide variety of electron donors, including both
easily biodegradable, low-molecular-weight substances
and slowly biodegradable cellulose materials. Many of
these electron donors can be converted in MFCs [5659].
The amount of electrons that can be derived from the
electron donor depends on the individual oxidation state
of the substance. Therefore, by controlling the type of
electron donor mobilized by the photosynthetic organisms,
and thus the oxidation state of the electron donor, energy
recovery can be improved in the MSC. For example, several
plants increase the release of low-molecular-weight com-
pounds, such as sugars, amino acids and phenolics, under

Figure 2. Schematic overview of a closed loop concept for an MSC with a
photobioreactor and a digester. (a) Photosynthesis by microalgae takes place in
the photobioreactor. (b) Bio-gas is produced from organic matter and is
transported from the photobioreactor to the digester. (c) At the anode of the
MFC, the remaining organic matter, which is transported from the digester to the
anode, is oxidized by electrochemically active bacteria. (d) At the cathode of the
MFC, oxygen, which is transported from the photobioreactor to the cathode, is
reduced to water. Reproduced with permission from [40].
Review Trends in Biotechnology January 2011, Vol. 29, No. 1
45
iron or zinc limitation conditions [50]. The remaining
challenge is to control plant exudation in such a way that
more reduced compounds are excreted.
Increase the CE of organic matter oxidation at the anode
The presence of other electron acceptors near the anode
possibly negatively affects the CE of photosynthetic meta-
bolites in MSCs. Photosynthetic metabolites may be oxi-
dized by mixed cultures using oxygen (aerobic
degradation), nitrate (nitrication), sulfate (sulfate reduc-
tion) or carbon dioxide (methanogenesis) as a nal electron
acceptor instead of the anode, which leads to a decrease in
CE [9,60,61]. An important source of alternative electron
acceptors in several MSC studies is nutrient media for
plants and microorganisms containing substantial
amounts of alternative electron acceptors, such as nitrate
and sulfate [10,12,14,15]. Such electron acceptors can be
replaced by more reduced components, thereby potentially
increasing the CE [10,12]. Oxygen is also a relevant alter-
native acceptor within PMFCs. Plant roots excrete oxygen,
which can be used by the microbial population present or
can produce internal currents. In the latter case, oxygen is
reduced within the anode compartment while using the
electrons derived from the electrochemically active bacte-
ria present in the same anode. Hence, these electrons do
not ow to the cathode, which thus decreases the power
output [61]. The total release of oxygen into the rhizo-
sphere can be decreased by decreasing the average root
length (e.g. using Glyceria maxima [10]) because oxygen
introduction into the rhizosphere decreases with root
length [62].
Decrease the pH gradient resistance of the fuel cell
Proton production in MFCs leads to acidication in the
anode compartment. Accumulation of protons creates a pH
gradient over the membrane, which results in a pH gradi-
ent potential loss (i.e. the pHgradient resistance) [7,63,64].
This phenomenon also occurs in MSCs [11]. Acidication
has been observed in a PMFC, which could be related to
current generation [14]. Although the pH in the rhizo-
sphere of the plants used is generally slightly acidic (pH
56), decreasing acidication will increase the energy re-
covery of this and other MSCs [14]. Several measures have
been proposed to decrease acidication in MFCs and these
could be translated to MSCs [7,65,66]. However, the nec-
essary energy input must also be considered because the
use of buffer or circulation thereof costs energy, and there-
fore might decrease the net power production.
Decrease the transport and ionic resistance of the fuel
cell
The total internal resistance of MSCs is a result of pH
gradient resistance, anode resistance, cathode resistance,
and ionic and transport resistance. These values have been
calculated for PMFCs [14,64]. Ionic resistance was de-
creased using a salt marsh species, thereby leading to
the possibility of current generation at higher ionic
strength [14]. In the same study it was observed that
transport resistance accounts for the greatest fraction of
the total internal resistance [14]. This was because the
anolyte was a stagnant water layer with an ion concentra-
tion gradient. This had to be overcome to drive cations from
the anode to the cathode. Mixing of the anolyte or circula-
tion of the catholyte over the anolyte will break down the
concentration gradient of cations and anions and thus
decrease the transport resistance.
Decrease the anode and cathode resistance of the fuel
cell
Similar to MFCs, MSCs have a specic anode and cathode
resistance that can be decreased to improve energy recov-
ery. General approaches, such as increasing the anode
surface area to decrease resistance, can be derived from
studies on similar bioelectrochemical systems [3,8,38,67],
which have been reviewed elsewhere [3,8,38].
MSCs with oxygen reduction on graphite show poor
performance because cathode resistance arises from
charge and mass transfer resistance [3,68,69]. Mass trans-
fer resistance can be decreased using air cathodes; howev-
er, long-term operation of air cathodes might be
challenging because oxygen transport could be hindered
by precipitates at the electrode, as observed in bio-cathodes
[70]. Cathode resistance can also be decreased by increas-
ing the surface area of the electrode or by enriching the
cathode with a biolm(so-called bio-cathodes) [3,39,68,71].
Bio-cathodes use populations of microorganisms or isolates
that catalyze the reduction of oxygen or other electron
acceptors, such as manganese and iron [68,7275].
The charge transfer resistance can also be decreased
using an electrocatalyst such as platinum (Pt), a solution
that has been demonstrated in several MSCs [19,32,41,67].
The challenge here is to decrease the dosage of platinum,
which is expensive [76]. Other MSCs use ferricyanide as a
nal electron acceptor; this is suitable for laboratory
experiments, but not feasible for large-scale systems be-
cause frequent replenishment is required [67].
Decrease the energy input of MSCs with
photobioreactors or with coastal marine ecosystems
MSCs that feed the MFC with seawater from coastal
marine ecosystems are limited by very dilute electron
donors. These can be concentrated for higher power output
[43]; however, achieving this with a lower energy input
remains a challenge. MSCs that use a photobioreactor or
MSCs with coastal marine ecosystems require an energy
input of 610 W/m
2
for processing the electron donor for the
MFC [3941,44]. This energy input can decrease the net
energy production of the MSC [39,43]. Thus, options for
improving the energy input efciency include decreasing
the energy input required and improving the photobior-
eactor productivity. Many valuable ideas on improvements
for photobioreactors have been published [77].
Prospects and future applications
We have shown that MSC technology is advancing, with
the most promising MSCs using higher plants or photo-
trophic biolms. The basic principles of MSCs have been
demonstrated; now it is time to improve the systems for
real-life applications. Compared to conventional solar cells,
MSCs have some attractive properties that warrant fur-
ther development and will inuence future applications of
this technology [78]:
Review
Trends in Biotechnology January 2011, Vol. 29, No. 1
46
MSCs can produce not only electricity, but also a wide
range of fuels and chemicals; this is in contrast to solar
cells, which generate only electricity [3].
PMFCs can easily be incorporated into landscapes or
into urban areas, where they green the city. For
example, PMFCs can be combined with green roofs to
create electricity-producing green roofs powering up to a
third of a modern household (Box 2).
Both photosynthetic and electrochemical reactions are
carried out by a continuously growing population of
microorganisms. This makes the system capable of self-
repair, conferring a longer lifetime and lowmaintenance.
Another advantage of the use of reproducing organisms
is that there is no need for special catalysts that are
either costly or toxic [78]. Thus, MSCs can be applied in
natural surroundings with no risk of pollution.
MSCs have organic material as intermediate energy
carriers between the photosynthetic and electrochemi-
cal parts of the cell. This organic material accumulates
in the MSC so that electricity can be generated in the
dark [10,11,39].
Closed MSC systems can preserve nutrients for the
organisms, which can result in long-term, low-mainte-
nance power production.
Integrated PMFCs can add value to other applications,
such as greenhouses with food or ower production, or
rice paddy elds with rice production [12,13]. In
addition, wastewater and surface water treatment
can be integrated into PMFCs to supply extra organic
matter for energy production [3,10].
For real-life MSC application, MSCs need to compete
with other renewable energy systems. Several factors, such
as energy yield, cost and environmental benets, will all
inuence the outcome of this competition (Box 3). There are
promising possibilities for application of MSCs according
to the best long-term power output of 50 mW/m
2
(Table 1).
For example, meteorological sensors for temperature, pres-
sure and humidity requiring 24 mW were installed on a
buoy and powered by a sediment MFC [79]. We expect that
these sensors and other applications that require low
amounts of power, such as LED lights, could be operated
using MSCs.
Acknowledgements
This research received funding from the European Community Seventh
Framework Programme FP7/2007-2013 under grant agreement no.
226532. In addition, work was funded by SenterNovem, the Dutch
governmental agency for sustainability and innovation from the Ministry
of Economic Affairs (grant no. EOSLT06020) and NUON. We thank Nora
Sutton, Marc Spiller, Jan Arends and the anonymous reviewers for their
valuable comments on the manuscript.
References
1 Imhoff, M.L. et al. (2004) Global patterns in human consumption of net
primary production. Nature 429, 870873
2 Solomon, S. et al. (2007) Climate Change 2007: The Physical Science
Basis, Contribution of Working Group I to the Fourth Assessment
Report of the Intergovernmental Panel on Climate Change, IPCC
3 Hamelers, H.V.M. et al. (2010) New applications and performance of
bioelectrochemical systems. Appl. Microbiol. Biotechnol. 85, 16731685
4 Steinbusch, K.J.J. et al. (2010) Bioelectrochemical ethanol production
through mediated acetate reduction by mixed cultures. Environ. Sci.
Technol. 44, 513517
5 Rozendal, R.A. et al. (2006) Principle and perspectives of hydrogen
production through biocatalyzed electrolysis. Int. J. Hydrogen Energy
31, 16321640
Box 3. Trade-off between PMFCs, wind turbines and solar
panels
If we focus primarily on energy production, the use of PMFCs or
phototrophic biofilms might be an alternative to photovoltaic solar
panels or wind turbines to create energy-producing landscapes. As
opposed to other alternative renewable electricity sources, PMFCs
offer the opportunity to increase both the aesthetic value and the
biodiversity of such landscapes. However, photovoltaic solar panels
and wind turbines can achieve higher power yields; thus, a cost
benefit analysis is required when considering implementation of a
renewable electricity technology [87].
When applied in a natural environment, PMFC power yield is
estimated to be a maximum of 1.6 MW/km
2
(Box 1). Whereas wind
turbines could generate 57.7 MW/km
2
on a typical wind farm in
Europe [88], solar panels could generate 4.57.5 MW/km
2
under
Western European conditions (solar radiation 150 W/m
2
, PCE 15
25%; the tilted position of a solar panel thus uses 2.5 m
2
of land per
m
2
of solar panel) [78]. In summary, the power output of wind farms
and solar farms will be three- to fivefold higher than that of PMFCs.
With an increasing need for electricity and in light of the European
political goal of generating 20% of its energy need in 2020 from
renewable sources, pressure on high-energy-yield per surface area
is increasing [89]. However, the environmental impact of both wind
turbines (avian mortality, visual impact, noise, electromagnetic
interference) and solar panels (visual impact, loss of green space
and biodiversity, increasing dark surface, use of polluting metals) is
large and is a source of societal debate [78,89]. PMFCs could offer an
opportunity for electricity generation while sustaining the natural
environment at locations where wind turbines or solar panels are
not desirable. Future integration of PMFCs into closed systems
could provide 24 h/day electricity generation without the use of
scarce materials and with nutrient preservation.
Box 2. The electricity-producing green roof
One of the most promising PMFC applications is a green roof
because it can combine the advantages of these roofs with
electricity generation by the PMFC. Green roofs are used all over
the world, especially in cities, and offer a myriad of advantages: (i)
storm-water runoff retention; (ii) high aesthetic value; (iii) increased
biodiversity; (iv) improvements in air quality; (v) building insulation;
and (vi) mitigation of urban heat islands (decrease in temperature
within cities, which have higher temperatures than rural surround-
ing areas) [8385]. When applying a PMFC to a green roof,
decentralized electricity production can be added to these advan-
tages. On a flat roof of 50 m
2
a reasonably sized roof in the
Netherlands 150 W could be continuously produced when the
proposed maximum of 3.2 W/m
2
is reached (Box 1). Assuming an
average electricity need of 500 W [86], a green roof could provide
approximately one-third of a households electricity need. More-
over, energy use by the household will decrease owing to the
insulation capacity of the green roof, so the PMFC power could be
expected to account for a larger proportion of the households
energy need. At an electricity price of s0.25/kWh, a 50-m
2
electricity-
producing green roof could potentially save a household s330 per
year.
To integrate a PMFC into a green roof, several bottlenecks still
have to be overcome. The plants in a PMFC need to be submerged,
so water retention on the green roof becomes more important.
Consequently, the weight of the roof will increase, which might
require a fortified building construction. Moreover, current labora-
tory set-ups are built with a lot of materials, leading to high costs
associated with a scaled-up system. A detailed design for an
electricity-producing green roof is therefore very important as it
will determine both the weight and costs of the system. The current
state of this technology does not enable us to propose a specific
design yet. Regardless of the challenges, PMFC integration with a
green roof offers the consumer an opportunity to produce electricity
while improving the quality of the urban environment.
Review Trends in Biotechnology January 2011, Vol. 29, No. 1
47
6 Kim, B.H. et al. (1999) Direct electrode reaction of Fe(III)-reducing
bacterium, Shewanella putrefaciens. J. Microbiol. Biotechnol. 9, 127
131
7 Rozendal, R.A. et al. (2008) Towards practical implementation of
bioelectrochemical wastewater treatment. Trends Biotechnol. 26,
450459
8 Pham, T.H. et al. (2009) Bioanode performance in bioelectrochemical
systems: recent improvements and prospects. Trends Biotechnol. 27,
168178
9 Rabaey, K. and Verstraete, W. (2005) Microbial fuel cells: novel
biotechnology for energy generation. Trends Biotechnol. 23, 291298
10 Strik, D.P.B.T.B. et al. (2008) Green electricity production with living
plants and bacteria in a fuel cell. Int. J. Energy Res. 32, 870876
11 Strik, D.P.B.T.B. et al. (2010) Solar energy powered microbial fuel cell
with a reversible bioelectrode. Environ. Sci. Technol. 44, 532537
12 De Schamphelaire, L. et al. (2008) Microbial fuel cells generating
electricity from rhizodeposits of rice plants. Environ. Sci. Technol.
42, 30533058
13 Kaku, N. et al. (2008) Plant/microbe cooperation for electricity
generation in a rice paddy eld. Appl. Microbiol. Biotechnol. 79, 4349
14 Timmers, R.A. et al. (2010) Long-termperformance of a plant microbial
fuel cell with Spartina anglica. Appl. Microbiol. Biotechnol. 86, 973
981
15 Helder, M. et al. (2010) Concurrent bio-electricity and biomass
production in three plantmicrobial fuel cells using Spartina
anglica, Arundinella anomala and Arundo donax. Bioresour.
Technol. 101, 35413547
16 Takanezawa, K. et al. (2010) Factors affecting electric output fromrice-
paddy microbial fuel cells. Biosci. Biotechnol. Biochem. 74, 12711273
17 De Schamphelaire, L. et al. (2010) Microbial community analysis of
anodes from sediment microbial fuel cells powered by rhizodeposits of
living rice plants. Appl. Environ. Microbiol. 76, 20022008
18 Logan, B.E. and Regan, J.M. (2006) Microbial fuel cells challenges
and applications. Environ. Sci. Technol. 40, 51725180
19 Zou, Y. et al. (2009) Photosynthetic microbial fuel cells with positive
light response. Biotechnol. Bioeng. 104, 939946
20 Lovley, D.R. (2008) The microbe electric: conversion of organic matter
to electricity. Curr. Opin. Biotechnol. 19, 564571
21 Herrero, A. and Flores, E. (2008) The Cyanobacteria: Molecular
Biology, Genomics, and Evolution, Caister Academic Press
22 Taiz, L. and Zeiger, E. (2006) Plant Physiology, Sinauer Associates
23 Lynch, J.M. (1990) The Rhizosphere, John Wiley & Sons
24 Richmond, A. (2004) Handbook of Microalgal Culture: Biotechnology
and Applied Phycology, Blackwell Publishing
25 Pabon Pereire, C.P. (2009) Anaerobic Digestion in Sustainable Biomass
Chains, Wageningen University
26 Weiland, P. (2010) Biogas production: current state and perspectives.
Appl. Microbiol. Biotechnol. 85, 849860
27 Berglund, M. and Borjesson, P. (2006) Assessment of energy
performance in the life-cycle of biogas production. Biomass
Bioenergy 30, 254266
28 Renewable energy technologies. Turkenburg, W.C. and Turkenburg,
W.C., eds), 2001.pp. 219272, UNDP
29 Holmes, D.E. et al. (2004) Microbial communities associated with
electrodes harvesting electricity from a variety of aquatic sediments.
Microb. Ecol. 48, 178190
30 De Schamphelaire, L. et al. (2008) Outlook for benets of sediment
microbial fuel cells with two bio-electrodes. Microb. Biotechnol. 1, 446
462
31 Bond, D.R. and Lovley, D.R. (2003) Electricity production by Geobacter
sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69,
15481555
32 Zou, Y. et al. (2010) Nanostructured polypyrrole-coated anode for sun-
powered microbial fuel cells. Bioelectrochemistry 79, 5056
33 Nishio, K. et al. (2010) Light/electricity conversion by a self-organized
photosynthetic biolm in a single-chamber reactor. Appl. Microbiol.
Biotechnol. 86, 957964
34 He, Z. et al. (2009) Self-sustained phototrophic microbial fuel cells
based on the synergistic cooperation between photosynthetic
microorganisms and heterotrophic bacteria. Environ. Sci. Technol.
43, 16481654
35 Malik, S. et al. (2009) A self-assembling self-repairing microbial
photoelectrochemical solar cell. Energy Environ. Sci. 2, 292298
36 Gorby, Y.A. et al. (2006) Electrically conductive bacterial nanowires
produced by Shewanella oneidensis strain MR-1 and other
microorganisms. Proc. Natl. Acad. Sci. U. S. A. 103, 1135811363
37 Brotas, V. and Catarino, F. (1995) Microphytobenthos primary
production of Tagus estuary intertidal ats (Portugal). Neth. J.
Aquat. Ecol. 29, 333339
38 Sleutels, T.H.J.A. et al. (2009) Improved performance of porous bio-
anodes in microbial electrolysis cells by enhancing mass and charge
transport. Int. J. Hydrogen Energy 34, 96559661
39 Strik, D.P.B.T.B. et al. (2008) Renewable sustainable biocatalyzed
electricity production in a photosynthetic algal microbial fuel cell
(PAMFC). Appl. Microbiol. Biotechnol. 81, 659668
40 De Schamphelaire, L. and Verstraete, W. (2009) Revival of the
biological sunlight-to-biogas energy conversion system. Biotechnol.
Bioeng. 103, 296304
41 Velasquez-Orta, S.B. et al. (2009) Energy from algae using microbial
fuel cells. Biotechnol. Bioeng. 103, 10681076
42 Ter Heijne, A. et al. (2006) A bipolar membrane combined with ferric
iron reduction as an efcient cathode system in microbial fuel cells.
Environ. Sci. Technol. 40, 52005205
43 Girguis, P.R. et al. (2010) Harnessing energy from marine productivity
using bioelectrochemical systems. Curr. Opin. Biotechnol. 21, 252
258
44 Reimers, C.E. et al. (2007) Substrate degradation kinetics,
microbial diversity, and current efciency of microbial fuel cells
supplied with marine plankton. Appl. Environ. Microbiol. 73, 7029
7040
45 Martin, J.H. et al. (1987) VERTEX: carbon cycling in the northeast
Pacic. Deep Sea Res. A Oceanogr. Res. Pap. 34, 267285
46 Rosenbaum, M. et al. (2005) In situ electrooxidation of photobiological
hydrogen in a photobioelectrochemical fuel cell based on Rhodobacter
sphaeroides. Environ. Sci. Technol. 39, 63286333
47 Cho, Y.K. et al. (2008) Development of a solar-powered microbial fuel
cell. J. Appl. Microbiol. 104, 640650
48 Harnisch, F. et al. (2009) Electrocatalytic and corrosion behaviour of
tungsten carbide in near-neutral pH electrolytes. Appl. Catal. B
Environ. 87, 6369
49 Berk, R.S. and Caneld, J.H. (1964) Bioelectrochemical energy
conversion. Appl. Microbiol. 12, 1012
50 Neumann, G. (2007) Root exudates and nutrient cycling. In Nutrient
Cycling in Terrestrial Ecosystems (Soil Biology Vol. 10) (Marschner, P.
and Rengel, Z., eds), pp. 123157, Springer-Verlag
51 Bais, H.P. et al. (2006) The role of root exudates in rhizosphere
interactions with plants and other organisms. Annu. Rev. Plant
Biol. 57, 233266
52 Grayston, S.J. et al. (1997) Rhizosphere carbon ow in trees, in
comparison with annual plants: the importance of root exudation
and its impact on microbial activity and nutrient availability. Appl.
Soil Ecol. 5, 2956
53 Fernandes, T.V. et al. (2009) Effects of thermo-chemical pre-treatment
on anaerobic biodegradability and hydrolysis of lignocellulosic
biomass. Bioresour. Technol. 100, 25752579
54 Aelterman, P. et al. (2008) Loading rate and external resistance control
the electricity generation of microbial fuel cells with different three-
dimensional anodes. Bioresour. Technol. 99, 88958902
55 Lyon, D.Y. et al. (2010) Is resistance futile? Changing external
resistance does not improve microbial fuel cell performance.
Bioelectrochemistry 78, 27
56 Feng, Y. et al. (2009) Electricity generation from corn stover by
cellulose degradation bacteria and exoelectrogenic bacteria. Huan
Jing Ke Xue 29, 22952299
57 Ren, Z. et al. (2008) Electricity production and microbial biolm
characterization in cellulose-fed microbial fuel cells. Water Sci.
Technol. 58, 617622
58 Rezaei, F. et al. (2008) Enzymatic hydrolysis of cellulose coupled with
electricity generation in a microbial fuel cell. Biotechnol. Bioeng. 101,
11631169
59 Pant, D. et al. (2010) A review of the substrates used in microbial fuel
cells (MFCs) for sustainable energy production. Bioresour. Technol.
101, 15331543
60 Virdis, B. et al. (2009) Electron uxes in a microbial fuel cell performing
carbon and nitrogen removal. Environ. Sci. Technol. 43, 5144
5149
Review
Trends in Biotechnology January 2011, Vol. 29, No. 1
48
61 Harnisch, F. and Schroder, U. (2009) Selectivity versus mobility:
separation of anode and cathode in microbial bioelectrochemical
systems. ChemSusChem 2, 921926
62 Soukup, A. et al. (2007) Apoplastic barriers to radial oxygen loss and
solute penetration: A chemical and functional comparison of the
exodermis of two wetland species, Phragmites australis and Glyceria
maxima. New Phytol. 173, 264278
63 Rozendal, R.A. et al. (2008) Effect of the type of ion exchange membrane
on performance, ion transport, and pH in biocatalyzed electrolysis of
wastewater. Water Sci. Technol. 57, 17571762
64 Sleutels, T.H.J.A. et al. (2009) Ion transport resistance in microbial
electrolysis cells with anion and cation exchange membranes. Int. J.
Hydrogen Energy 34, 36123620
65 Jeremiasse, A.W. et al. (2009) Use of biocompatible buffers to reduce
the concentration overpotential for hydrogen evolution. Environ. Sci.
Technol. 43, 68826887
66 Rozendal, R.A. et al. (2006) Effects of membrane cation transport on pH
and microbial fuel cell performance. Environ. Sci. Technol. 40, 5206
5211
67 Logan, B.E. et al. (2006) Microbial fuel cells: Methodology and
technology. Environ. Sci. Technol. 40, 51815192
68 He, Z. and Angenent, L.T. (2006) Application of bacterial biocathodes in
microbial fuel cells. Electroanalysis 18, 20092015
69 Ter Heijne, A. et al. (2010) Cathode potential and mass transfer
determine performance of oxygen reducing biocathodes in microbial
fuel cells. Environ. Sci. Technol. 44, 71517156
70 Jeremiasse, A.W. et al. (2010) Microbial electrolysis cell with a
microbial biocathode. Bioelectrochemistry 78, 3943
71 Freguia, S. et al. (2010) Electron transfer pathways in microbial oxygen
biocathodes. Electrochim. Acta 55, 813818
72 Bergel, A. et al. (2005) Catalysis of oxygen reduction in PEMfuel cell by
seawater biolm. Electrochem. Commun. 7, 900904
73 Rabaey, K. et al. (2008) Cathodic oxygen reduction catalyzed by
bacteria in microbial fuel cells. ISME J. 2, 519527
74 Ter Heijne, A. et al. (2007) Microbial fuel cell operation with continuous
biological ferrous iron oxidation of the catholyte. Environ. Sci. Technol.
41, 41304134
75 Aelterman, P. et al. (2009) Microbial fuel cells operated with iron-
chelated air cathodes. Electrochim. Acta 54, 57545760
76 Rosenbaum, M. et al. (2010) Light energy to bioelectricity:
photosynthetic microbial fuel cells. Curr. Opin. Biotechnol. 21, 259
264
77 Janssen, M. et al. (2003) Enclosed outdoor photobioreactors: light
regime, photosynthetic efciency, scale-up, and future prospects.
Biotechnol. Bioeng. 81, 193210
78 Kazmerski, L.L. (2006) Solar photovoltaics R&D at the tipping point: a
2005 technology overview. J. Electron Spectrosc. Relat. Phenom. 150,
105135
79 Tender, L.M. et al. (2008) The rst demonstration of a microbial fuel
cell as a viable power supply: powering a meteorological buoy. J. Power
Sources 179, 571575
80 Fontoynont, M. et al. (1998) Satel-Light: a www server which provides
high quality daylight and solar radiation data for western and central
Europe. In Proceedings of the 9th Conference on Satellite Meteorology
and Oceanography, Paris, pp. 434435, Eumetstat
81 Whipps, J.M. and Lynch, J.M. (1985) Energy losses by the plant in
rhizodeposition. Annu. Proc. Phytochem. Soc. Eur. 26, 5971
82 Hamelers, H.V.M. et al. (2011) ButlerVolmerMonod model for
describing bio-anode polarization curves. Bioresour. Technol. 102,
381387
83 Niachou, A. et al. (2001) Analysis of the green roof thermal properties
and investigation of its energy performance. Energy Build. 33, 719729
84 Getter, K.L. et al. (2009) Carbon sequestration potential of extensive
green roofs. Environ. Sci. Technol. 43, 75647570
85 Wong, N.H. et al. (2003) Investigation of thermal benets of rooftop
garden in the tropical environment. Build. Environ. 38, 261270
86 Arkesteijn, K. and Oerlemans, L. (2005) The early adoption of green
power by Dutch households. An empirical exploration of factors
inuencing the early adoption of green electricity for domestic
purposes. Energy Policy 33, 183196
87 Goldemberg, J. et al. (eds), (2004) World Energy Assessment. Energy
and the Challenge of Sustainability, UNDP
88 McGowan, J.G. and Connors, S.R. (2000) Windpower: a turn of the
century review. Annu. Rev. Energy Environ. 25, 147197
89 Campoccia, A. et al. (2009) Comparative analysis of different
supporting measures for the production of electrical energy by solar
PV and wind systems: four representative European cases. Sol. Energy
83, 287297
Review Trends in Biotechnology January 2011, Vol. 29, No. 1
49

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