Microbial fuel cells: novel microbial physiologies and
engineering approaches
Derek R Lovley
The possibility of generating electricity with microbial fuel cells
has been recognized for some time, but practical applications
have been slow to develop. The recent development of a
microbial fuel cell that can harvest electricity from the organic
matter stored in marine sediments has demonstrated the
feasibility of producing useful amounts of electricity in remote
environments. Further study of these systems has led to the
discovery of microorganisms that conserve energy to support
their growth by completely oxidizing organic compounds to
carbon dioxide with direct electron transfer to electrodes. This
suggests that self-sustaining microbial fuel cells that can
effectively convert a diverse range of waste organic matter or
renewable biomass to electricity are feasible. Significant
progress has recently been made to increase the power output
of systems designed to convert organic wastes to electricity,
but substantial additional optimization will be required for largescale electricity production.
Addresses
Department of Microbiology, University of Massachusetts, Amherst,
MA 01003, USA
Corresponding author: Lovley, Derek R ([email protected])
Current Opinion in Biotechnology 2006, 17:327–332
This review comes from a themed issue on
Energy biotechnology
Edited by Jonathan R Mielenz
Available online 5th May 2006
0958-1669/$ – see front matter
# 2006 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.copbio.2006.04.006
Introduction
As supplies of fossil fuels dwindle and concerns about
continued contributions of additional carbon dioxide to
the atmosphere intensify, there is an increasing need for
new sources of energy from renewable carbon-neutral
sources with minimal negative environmental impact.
Producing electricity from organic matter with microbial
fuel cells is a concept that arguably dates back almost 100
years [1]. As recently reviewed [1], the basic principals of
microbial fuel cells were established some time ago in
pioneering studies by groups led by Bennetto, Kim,
Zeikus and others.
In the most general sense, microbial fuel cells function by
oxidizing an electron donor with electron transfer to the
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anode under anoxic conditions (Figure 1). The electron
donor can be a reduced product of microbial metabolism
or an added artificial mediator that facilitates electron
transfer by accepting electrons from the microbes and
donating them to the anode. In some instances the
microorganisms can produce their own soluble electron
transfer mediator. Alternatively, some microorganisms
can directly transfer electrons to the anode surface. Electrons donated to the anode pass through a resistor or other
type of electrical device to the cathode. The cathode may
be exposed to the air or submerged in aerobic water.
Protons released from oxidation of the organic matter
migrate to the cathode, often through a cation-selective
membrane that limits diffusion of oxygen into the anode
chamber. Electrons, protons and oxygen combine at the
cathode surface to form water.
Although interest in microbial fuel cells was relatively
high in the 1960s, the study of microbial fuel cells waned
as the cost of other energy sources remained low and the
available microbial fuel cells lacked efficiency and longterm stability. However, in the past three to four years
there has been a resurgence in microbial fuel cell
research. As detailed below, advances have included
the development of what could be the first microbial fuel
cell that can out compete more conventional power
sources for its designated application, significant efforts
to better engineer systems for harvesting electricity from
organic wastes, and the discovery of microorganisms with
enhanced capacities for sustained, efficient electricity
production.
BUG Juice
One of the most exciting discoveries in the past few years
in microbial fuel cell research was the development by
Reimers and Tender of a microbial fuel cell that can
harvest electricity from the organic matter in aquatic
sediments [2–4]. These systems are now known as
Benthic Unattended Generators or BUGs (http://
www.nrl.navy.mil/code6900/bug/). BUGs are being
designed for powering electronic devices in remote locations, such as the bottom of the ocean, where it would be
expensive and technically difficult to routinely exchange
traditional batteries [3,5]. BUGs consist of an anode
buried in anoxic marine sediments connected to a cathode suspended in the overlying aerobic water (Figure 2).
Similar designs could potentially power electronic
devices in remote terrestrial locations and could even
eventually be modified to harvest electricity from other
sources such as compost piles, septic tanks and waste
lagoons.
Current Opinion in Biotechnology 2006, 17:327–332
328 Energy biotechnology
Figure 1
Generalized diagram of a microbial fuel cell. This fuel cell is shown with an ‘air-breathing’ cathode based on the pioneering work of Park
and Zeikus [52]. In many instances, however, the cathode is immersed in water containing dissolved oxygen. Electrons derived from the
microbial oxidation of organic compounds are transferred to the anode by direct electron transfer from the microorganisms or electron transfer
can be mediated by a soluble electron shuttle, which is either added to the culture or produced by the microbe itself. Electrons flow from the
anode to the cathode through wires. Protons produced from organic matter oxidation pass through the cation-selective membrane and combine
with electrons and oxygen at the cathode surface to produce water.
It was initially proposed that the microbes degrading
organic matter in sediments produced reduced end products, such as sulfide, Fe (II) and reduced humic substances, which then donated electrons to the electrodes
[2]. This hypothesis was consistent with the reactions
known to occur in the microbial fuel cells at the time, in
which the reduced end products of microbial metabolism
or reduced artificial mediators were the direct source
of electrons [6]. However, subsequent microbiological
analysis has now suggested that microorganisms are more
directly involved in electron transfer to the anode of
BUGs.
Molecular analysis of the microbial community on anode
surfaces revealed that microorganisms in the family Geobacteraceae accounted for about half of the microorganisms, but there was no similar enrichment of
Geobacteraceae on graphite buried in the sediment that
was not connected to a cathode [3,7,8]. In marine sediments, Desulfuromonas species, which prefer marine salinities, predominated on the anodes, whereas Geobacter
species, which prefer freshwater, were most abundant on
Current Opinion in Biotechnology 2006, 17:327–332
electrodes buried in freshwater sediments. Geobacter species were also highly enriched on electrodes harvesting
electricity from other organic material, such as swine
waste (KB Gregory et al. unpublished). Pure culture
studies demonstrated that Geobacteraceae are capable of
conserving energy to support growth by completely oxidizing acetate and other organic compounds to carbon
dioxide with an electrode serving as the sole electron
acceptor [7,9,10]. The ability of Geobacteraceae to produce
electricity in this manner is probably related to their
ability to transfer electrons outside the cell onto Fe(III)
and Mn(IV) oxides, which are also insoluble, extracellular
electron acceptors [11].
The oxidation of sediment organic matter coupled to the
reduction of Fe(III) and Mn(IV) oxides is catalyzed by a
consortia of microorganisms. Some microorganisms break
down the complex assemblage of organic matter to produce fermentation products, such as acetate, and other
potential electron donors for Geobacteraceae, such as
aromatic compounds and long-chain fatty acids. The
Geobacteraceae can then oxidize these compounds with
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Microbial fuel cells Lovley 329
Figure 2
Model for electricity production in sediment microbial fuel cells. Complex organic matter in the sediments is broken down by various hydrolytic
enzymes and fermentative microorganisms to acetate and other electron donors, which Geobacteraceae can then oxidize to carbon dioxide
with electron transfer to the anode.
the reduction of Fe(III) or Mn(IV) [11]. It is assumed that
a similar microbial food chain, with anodes substituting
for the Fe(III) and Mn(IV) that Geobacteraceae would
naturally use, provides electrons to BUGs (Figure 2).
However, the microbiology of BUG anodes could be more
complex in some environments. In freshwater environments, Geothrix species, although not as abundant as
Geobacter species, might contribute to electricity production [8,12]. In some sulfide-rich sediments, microorganisms with 16S rRNA sequences closely related to known
Desulfobulbus species predominate on the anodes [8]. The
likely reason for this is that sulfide abiotically reacts with
the electrode to form S8, the elemental form of sulfur, and
Desulfobulbus species then oxidize the S8 to sulfate using
the anode as the electron acceptor [13].
A better understanding of how Geobacteraceae and other
organisms that colonize the anodes of BUGS transfer
electrons to the anode surface could facilitate further
optimization of these systems. Electron transfer to electrodes in Geobacteraceae has primarily been studied with
Geobacter sulfurreducens, because this organism is closely
related to the Geobacteraceae that colonize electrodes in
sediments and the complete genome sequence [14], a
genetic system [15] and whole-genome DNA microarrays
[16] are available for this microorganism. Furthermore, it
is possible to track the metabolism of G. sulfurreducens
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growing on electrodes by monitoring the gene transcript
levels. For example, Geobacteraceae possess a unique,
eukaryotic-like citrate synthase that catalyzes a key step
in acetate oxidation [17]. Levels of transcripts for citrate
synthase increased in cells of G. sulfurreducens growing on
electrodes as current production from acetate oxidation
increased, demonstrating a link between transcript levels
and metabolism on electrodes [18]. A combination of
gene expression and genetic studies have recently indicated that many of the key components involved in
extracellular electron transfer to Fe(III) oxides, such as
the outer-membrane c-type cytochromes OmcS and
OmcE [19], are also involved in electron transfer to
electrodes [20]. Surprisingly, under conditions that mimic
the BUG system, the electrically conductive pili that are
essential for electron transfer to Fe(III) oxides [21] were
not required for electron transfer to electrodes [20].
Another route to increasing electricity production could
be to alter central metabolism to increase rates of respiration. With the genome-based in silico model of G. sulfurreducens [22] it has been possible to predict strategies for
increasing respiration rates and thus to provide increased
electricity production.
Large-scale conversion of organic wastes
and renewable biomass to electricity
One of the most active areas of microbial fuel cell research
in the past few years has been in the further development
Current Opinion in Biotechnology 2006, 17:327–332
330 Energy biotechnology
of fuel cells designed to produce power from organic
wastes such as sewage. Like BUGs, the concept is to
rely on the microorganisms naturally present in the waste
organic matter to transfer electrons to the anode. Unlike
BUGs, in which there is generally a predominance of the
same types of microorganisms on the anode surface
regardless of the site of deployment, the microbiology
of prototypes for waste water treatment appears to be
highly dependent upon the design and operational parameters of the system. For example, in a system harvesting
electricity under highly anoxic conditions, Geobacter species accounted for over 70% of the microbes on anode
surfaces and were considered to be the predominant
organisms involved in electricity production (KB Gregory
et al. unpublished). However, in other systems, in which
the reactor design permits substantial leakage of oxygen
into the anode chamber, organisms more tolerant to
oxygen exposure can predominate [23,24,25].
Whether the microbial fuel cells are run in batch or flowthrough mode can also impact not only on the type of
microorganisms present, but also on the mechanisms by
which electrons are transferred to the anode. For example, in a batch system converting glucose to electricity,
there appeared to be selection for microorganisms producing compounds that acted as electron shuttles to promote
electron transfer to the electrode surface [24]. Although a
strain of Pseudomonas aeruginosa capable of utilizing glucose and producing an electron shuttle was isolated from
this system, the isolated strain was inefficient in converting glucose to electricity owing, at least in part, to the fact
that it only incompletely oxidized glucose to fatty acids
[26]. Therefore, it is not clear what microorganisms were
responsible for the high rates of power production in the
mixed community.
The production of electron shuttles is much less likely to
be an important strategy for electron transfer to anodes in
flow-through systems [27] or other types of open systems
in which there is a frequent change of the fluid around the
anode. This is because, in an environment in which the
shuttle might be rapidly lost to the external environment,
the energetic cost of biosynthesizing an electron shuttle
puts an electron-shuttle-producing microorganism at a
severe disadvantage compared with microorganisms that
directly transfer electrons to the anode (Box 1).
Most recent studies on the conversion of organic wastes to
electricity have focused on the engineering challenges of
developing such systems: the composition, surface area
and positioning of the anodes, cathodes and cation-selective membrane [28–31,32,33,34]; the ionic strength of
the medium [28,35]; and flow-through characteristics
[27,32,36]. These studies included very little microbiology and thus the reader is referred to recent reviews
[37–39] for more in-depth coverage of this subject. In
some instances, these innovations have substantially
Current Opinion in Biotechnology 2006, 17:327–332
Box 1 The metabolic diversity of electricity-producing microbes
For many applications microbial fuel cells rely on the selection of
electricity-producing microorganisms from the natural community
of microbes in the organic source material. However, pure culture
studies are useful to evaluate the mechanisms of electricity
production and strategies for optimizing this process [47].
For many years, pure culture microbial fuel cells were constructed
with organisms that required the addition of an artificial mediator to
promote electron transfer to the anode [6]. Such microorganisms are
probably not relevant to electricity production from aquatic sediments or organic wastes, where artificial mediators are not added.
Some electricity-producing microorganisms, such as Shewanella
and Geothrix species, produce their own electron shuttles [11] and it
has been suggested that a microorganism producing an electron
shuttle will have the advantage that it can be positioned at a distance
from the electrode and yet still transfer electrons to the electrode
surface [26]. However, biosynthesizing an electron shuttle has a high
energetic cost [22] that cannot be recovered in open environments,
such as flow-through sewage treatment systems or aquatic
sediments, in which the shuttle could be rapidly lost from the
site of release. This might be one explanation why Geothrix species
appear to be at a disadvantage relative to Geobacter species, which
directly transfer electrons to electrodes, when competing for space
on the anode of sediment microbial fuel cells [12]. Likewise,
Shewanella species have not been reported to be important
components of fuel cells that harvest electricity from waste organic
matter or sediments. Additional reasons for this observation could be
that the substrates they utilize, such as lactate, are unlikely to be
central extracellular intermediates in the anaerobic degradation of
organic matter [11] and the fact that Shewanella species only
incompletely oxidize lactate to acetate on electrodes, leading to
inefficient electricity production [9,48]. Some other organisms that
have recently been studied in microbial fuel cells [49,50] also have
low efficiencies in the conversion of organic fuels to electricity;
however, efficient conversion of organic matter and not producing an
electron shuttle does not ensure competitiveness on anode surfaces.
Rhodoferax ferrireducens has the remarkable ability to completely
oxidize sugars to carbon dioxide with direct electron transfer to an
anode [51]. However, this organism has yet to be reported as
abundant on anodes harvesting electricity in sediment fuel cells. For
reasons yet to be fully evaluated, the combined activity of
fermentative microorganisms coupled with the oxidation of fermentation products by Geobacteraceae appears to be the more
competitive process.
increased power output; however, challenges remain.
In the flow-through systems that would be required to
treat large volumes of liquid waste, the highest power
outputs are less than 2 W per square meter of anode
surface, even when treating readily degradable pure
substrates such as glucose [32]. This power output is
unlikely to be sufficient to recover the power expended
in pumping the fluid through the system. Scaling of these
laboratory systems to the size that would be required to
handle large volumes of wastes also remains an issue.
Sensors
Systems based on the microorganism Shewanella show
promise as sensors for quantifying the biological oxygen
demand in sewage [40–42]. This concept might readily be
expanded to detect other compounds that can act as
electron donors for electricity production, such as hydrogen [9] or aromatic contaminants [7].
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Microbial fuel cells Lovley 331
Microbes on the cathode
References and recommended reading
Given the ability of Geobacter species to make an electrical
connection with graphite electrodes, it might not be
surprising that, if an electrode is poised at a negative
potential, Geobacter species can accept electrons from an
electrode [43]. When a negatively poised electrode was
placed in a sediment inoculum, nitrate was reduced and
there was an enrichment of Geobacter species on the
electrode surface [43]. In another study different, as
yet unidentified, organisms were enriched [44]. Pure
cultures of Geobacter species were able to reduce physiological electron acceptors such as nitrate and fumarate
with the electrode serving as the sole electron donor. A
poised electrode also promoted the reduction of soluble
U(VI) to insoluble U(IV) in uranium-contaminated subsurface sediments [45]. The U(IV) precipitated on the
electrode surface. Thus, reduction of U(VI) with electrodes could be a more preferable strategy for the bioremediation of uranium-contaminated subsurface
environments than the addition of organic electron
donors, because electrodes also provide a simple means
of removing the uranium from the ground [45]. Electrodes could conceivably be used to provide electrons for the
bioremediation of other contaminants, such as chlorinated
solvents and perchlorate.
Papers of particular interest, published within the annual period of
review, have been highlighted as:
Manganese-oxidizing microorganisms served as the catalysts in a novel cathode system that increased the
current by almost two orders of magnitude over plain
graphite electrodes in a microbial fuel cell [46].
Mn(IV) precipitated on the cathode is reduced to
Mn(II), which the manganese oxidizers recycle back to
Mn(IV).
Conclusions
Microorganisms that can couple the oxidation of organic
compounds to electron transfer to electrodes offer the
promise of self-sustaining systems that can effectively
convert waste organic matter and renewable biomass into
electricity. Oxidation of these recently fixed sources of
organic carbon does not contribute net carbon dioxide to
the atmosphere and, unlike hydrogen fuel cells, there is
no need for extensive pre-processing of the fuel or for
expensive catalysts. With the appropriate optimization,
microbial fuel cells might be able to power a wide range of
widely used devices. For example, there is ongoing
research on the potential for powering self-feeding robots
and even automobiles in this manner [1]. Another possibility is to use systems similar to BUGs for harvesting
electricity from domestic and agricultural wastes to provide a decentralized power source in extensive rural areas
not served by power grids in developing countries. However, significant optimization of microbial fuel cells will
be required for most applications. Further investigations
into the physiology and ecology of microbes that transfer
electrons to electrodes are essential to carry out these
optimizations in a rational manner.
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of special interest
of outstanding interest
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Current Opinion in Biotechnology 2006, 17:327–332
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