Environmental Microbiology Reports (2011) 3(1), 27–35
doi:10.1111/j.1758-2229.2010.00211.x
Minireview
Powering microbes with electricity: direct electron
transfer from electrodes to microbes
emi4_211
Derek R. Lovley*
Department of Microbiology, University of
Massachusetts, Amherst, MA 01003, USA.
Summary
The discovery of electrotrophs, microorganisms that
can directly accept electrons from electrodes for the
reduction of terminal electron acceptors, has spurred
the investigation of a wide range of potential applications. To date, only a handful of pure cultures have
been shown to be capable of electrotrophy, but this
process has also been inferred in many studies
with undefined consortia. Potential electron acceptors include: carbon dioxide, nitrate, metals, chlorinated compounds, organic acids, protons and
oxygen. Direct electron transfer from electrodes to
cells has many advantages over indirect electrical
stimulation of microbial metabolism via electron
shuttles or hydrogen production. Supplying electrons
with electrodes for the bioremediation of chlorinated
compounds, nitrate or toxic metals may be preferable
to adding organic electron donors or hydrogen to the
subsurface or bioreactors. The most transformative
application of electrotrophy may be microbial electrosynthesis in which carbon dioxide and water are
converted to multi-carbon organic compounds that
are released extracellularly. Coupling photovoltaic
technology with microbial electrosynthesis represents a novel photosynthesis strategy that avoids
many of the drawbacks of biomass-based strategies
for the production of transportation fuels and other
organic chemicals. The mechanisms for direct electron transfer from electrodes to microorganisms
warrant further investigation in order to optimize envisioned applications.
Received 15 June, 2010; accepted 21 July, 2010. *For correspondence. E-mail [email protected]; Tel. (+1) 413 545 9651;
Fax (+1) 413 545 1576.
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd
27..35
Introduction
Engineered microbial processes, such as the production
of fuels and other chemicals as well as bioremediation,
have traditionally relied on biomass-based organic feedstocks as the electron donor. However, photovoltaic technology is much more efficient in capturing solar energy
than photosynthesis, does not require arable land, and
avoids the introduction of excess nutrients and other pollutants associated with intensive agriculture. Like photovolatics, other major renewable forms of energy such as
wind, hydro and geothermal can also produce electricity.
Therefore, the possibility of powering beneficial microbial
processes with electricity is becoming increasingly attractive. As detailed below, this may be most effectively
accomplished by providing microorganisms with electrons
via direct electron transfer from electrodes, coupled to the
microbial reduction of various electron acceptors.
Microorganisms capable of directly accepting electrons
from electrodes have been referred to colloquially as
electrode-oxidizing bacteria (Lovley, 2008) just as microorganisms are referred to iron-oxidizing, sulfur-oxidizing
or methane-oxidizing microbes. A more formal designation may be electrotrophs in accordance with the standard
parlance of chemotrophs that oxidize chemical compounds in their environments (organotrophs oxidize
organic compounds; lithotrophs oxidize inorganics) and
phototrophs.
This review summarizes current knowledge on how
electrons can be directly transferred from electrodes to
microorganisms and the potential practical applications of
this novel form of microbial respiration in bioremediation,
bioenergy and chemical production.
Background on microbe–electrode interactions
Various reviews (Lovley, 2006; Debabov, 2008) have
recounted the last century of the study of microbe–
electrode interactions. The ability of microorganisms to
transfer electrons to electrodes without the addition of an
exogenous electron shuttling mediator was known from
the start (Potter, 1911), despite the often cited report
claiming that this phenomenon is a recent discovery.
28 D. R. Lovley
An important breakthrough in the understanding of
electron transfer to electrodes was the finding that nonfermentable substrates, such as acetate, could be oxidized to carbon dioxide with direct electron transfer to an
electrode serving as the sole electron acceptor (Bond
et al., 2002; Bond and Lovley, 2003). This demonstrated
for the first time that electron transfer to electrodes could
be a respiratory process because there is no possibility for
substrate-level phosphorylation with acetate as the electron donor under anaerobic conditions. These, and related
studies, also demonstrated for the first time that microorganisms could extract electrons from organic matter
and convert them to electric current with high (> 90%)
efficiencies.
The ability of microorganisms to respire and conserve
energy with an electrode serving as the sole electron
acceptor makes it feasible for electrode-reducing populations to be self-sustaining. This is significant because
one of the most commonly considered applications of
microbial electron transfer to electrodes is electrical
current production in microbial fuel cells (Lovley, 2008;
Logan, 2009). In these systems electrons transferred to
an electrode (the anode) under anaerobic conditions can
be conducted to another electrode (the cathode), typically
under aerobic conditions with the reduction of oxygen.
The current flow between the anode and the cathode
can power electronic devices. Unfortunately, various limitations other than the rates of microbial metabolism critically limit the power output of microbial fuel cells in
present designs (Logan, 2009) and have restricted their
likely short-term applications to powering electronic
devices in remote locations (Tender et al., 2008) and
accelerating the degradation of hydrocarbon contaminants in polluted sediments (Zhang et al., 2010).
In contrast to the long history of the study of direct
microbial electron transfer to electrodes, the history
of direct electron flow in the opposite direction, from
electrodes to microorganisms, is rather short with the first
report appearing in 2004 (Gregory et al., 2004). Prior to
this, as recently reviewed (Thrash and Coates, 2008),
there was substantial study on a wide diversity of redoxactive molecules that can function as electron shuttles,
accepting electrons from electrodes and delivering the
electrons to microorganisms to influence fermentation
patterns or promote the reduction of inorganic electron
acceptors. Alternatively, proton reduction to hydrogen gas
can be exploited to indirectly deliver electrons to microorganisms. After examining the available literature, Thrash
and Coates concluded that the electron-shuttling and
hydrogen-production approaches have serious limitations
(Thrash and Coates, 2008). Potential disadvantages of
producing hydrogen as an electron carrier include high
energy costs due to the low electrode potentials required
to generate hydrogen without expensive catalysts and the
generation of a highly insoluble, explosive gas, which
microorganisms may have difficulties in efficiently consuming (Aulenta et al., 2008). In environmental applications hydrogen production non-specifically stimulates
a diversity of forms of microbial respiration. Electron
shuttles can typically be reduced at higher electrode
potentials than protons, thus saving energy (Thrash and
Coates, 2008). However, electron shuttles add cost and
may lack long-term stability (Steinbusch et al., 2010). The
toxicity of many shuttles precludes their use in open environments and shuttles must be separated from products
and removed from discharge water in reactor applications. Both shuttles and hydrogen promote the proliferation of planktonic cells in contrast with the electrodeattached cells resulting from direct electron transfer.
Electrode-attached cells remain separate from products
and make it feasible to directly feed specific microorganisms in a defined location in environmental applications.
Thus, Thrash and Coates (2008) considered direct electron transfer from electrodes to microorganisms to be
the best long-term technology for providing electrons to
microorganisms.
The first evidence for direct electron transfer from electrodes to microorganisms came from studies with Geobacter species (Thrash and Coates, 2008). As detailed
below, a diversity of Geobacter species are now known to
reduce a variety of electron acceptors, including nitrate,
fumarate, U(VI) and chlorinated solvents as electron
acceptors. Data directly demonstrating or suggestive of
direct electron transfer from electrodes to additional
microorganisms and a wider diversity of electron acceptors is beginning to rapidly accumulate. This, in turn, is
leading to a number of envisioned applications.
Direct electron transfer from electrodes in detail
Devices for directly delivering electrons
to microorganisms
In order to fully understand direct electron transfer to
microorganisms and its potential applications, it is important to know how previous studies have directly supplied
electrons to microorganisms. Pure culture studies have
generally been carried out in reactors, which are referred
to here as electrotrophic reactors (Fig. 1).
Water is generally the source of electrons in electrotrophic reactors. Water is a convenient electron source
because it can readily be split with the release of oxygen
and protons at the anode surface (Fig. 1). In envisioned
large-scale applications, such as the industrial production
of fuels and chemicals, water is the only conceivable
inexpensive, readily available, abundant electron source.
Water is also the most likely electron source for environmental applications. The possibility of microorganisms
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology Reports, 3, 27–35
Feeding Microbes Electricity 29
Evidence for direct electron transfer
in Geobacter species
Fig. 1. General strategy for supplying electrotrophic
microorganisms with electrons for the reduction of various electron
acceptors that have been documented in pure culture. Water is the
electron donor of choice at the anode for many applications, but
electrons may be supplied with other strategies, such as microbial
oxidation of organic compounds coupled to electron transfer to the
anode.
oxidizing organic matter with electron transfer to anodes,
as in a microbial fuel cell, is frequently proposed as an
alternative electron source. However, until the present
issues with low current outputs (Logan, 2009) and problems with scaling up these systems (Dewan et al., 2008)
are resolved, supplying electrons from organic matter at
significant rates will not be possible in anything other than
small lab-scale demonstrations.
In electrotrophic reactors, electronics are used to
poise the cathode at a negative potential (typically -300
to -400 mV versus standard hydrogen electrode) low
enough to support anaerobic respiration, but too high for
significant hydrogen production. Electrons are derived
from water at the anode with the production of oxygen and
protons. The anode and cathode chambers can be separated with a selective membrane to limit oxygen diffusion
into the cathode chamber while promoting proton/charge
balance. The source of electrical power is typically a standard electrical outlet, but devices have been built that
permit these systems to be run with solar power, an important consideration for future bioenergy and chemical production applications (Nevin et al., 2010).
Solar powered units have been deployed in bioremediation field applications using arrangements that are
similar to the field deployment of microbial fuel cells that
can monitor microbial metabolism in subsurface environments (Williams et al., 2010). The basic principle is the
same as the laboratory electrotrophic units. The anode is
placed in the soil at the surface and the cathode is
deployed at depth. As detailed below, powering subsurface bioremediation with solar-powered cathode systems
offers the potential advantages of carrying out bioremediation in a sustainable, low-maintenance manner.
When a freshwater sediment inoculum was added into a
standard electrotrophic reactor in which the cathode
served as the sole electron donor and nitrate was the
potential electron acceptor, nitrate was reduced to nitrite
with a stoichiometry of electron consumption and nitrate
reduction consistent with the electrode serving as the sole
electron donor for nitrate reduction (Gregory et al., 2004).
The microbial community attached to the electrode was
highly enriched in Geobacter species. Pure cultures of
Geobacter metallireducens carried out a similar electrodedriven nitrate reduction. Geobacter sulfurreducens, which
is not capable of nitrate reduction but can reduce fumarate, reduced fumarate to succinate with an electrode as
the sole electron donor. The possibility of indirect electron
transfer mediated by the reduction of protons to hydrogen followed by the consumption of hydrogen by the
Geobacter species could be ruled out because: (i) the
electrode was poised at a potential that was too high for
appreciable hydrogen production, (ii) G. metallireducens
is not able to use hydrogen as an electron donor, and (iii)
a strain in of G. sulfurreducens in which a gene for the
hydrogenase required for hydrogen uptake had been
deleted reduced fumarate as well as wild-type cells
(Gregory et al., 2004).
The finding that the capacity for current consumption
by G. sulfurreducens increased over time with repeated
additions of fumarate suggested that energy might be
conserved to support growth from direct electron transfer
from electrodes, but more definitive studies were not
conducted. Geobacter species have previously been
shown to oxidize other extracellular reduced species,
such as reduced humic substances (Lovley et al., 1999),
but growth with those electron donors was also not demonstrated. Further evaluation of the growth yields possible
from electron transfer from electrodes is a high research
priority.
Growth with an electrode serving as an electron donor
is theoretically possible when common electron acceptors
are reduced on the inner side of the inner membrane or in
the cytoplasm (Fig. 2). This is because the reduction of
these electron acceptors consumes protons for the production of the reduced end product. Consumption of
protons within the cytoplasm will result in a proton gradient across the inner membrane.
Also, unknown are the mechanisms for electron
exchange between electrodes and Geobacter species
when electrodes serve as the electron donor. When G.
sulfurreducens oxidizes acetate with electron transfer to
electrodes it forms thick (> 50 mm) biofilms and even cells
at this substantial distance from the anode are considered
to contribute to current production (Reguera et al., 2006;
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology Reports, 3, 27–35
30 D. R. Lovley
Fig. 2. Proposed mechanism for energy conservation with an
electrode serving as the sole electron donor and carbon dioxide
as the sole electron acceptor. The reduction of other electron
acceptors on the cytoplasmic side of the inner membrane will also
consume protons, leading to a proton gradient across the inner
membrane.
Lovley, 2008; Franks et al., 2010). The working model for
electron transfer to the anode in thick G. sulfurreducens
biofilms is that conductive pili (Reguera et al., 2005) are
responsible for electron transfer through the bulk of the
biofilm (Reguera et al., 2006; Lovley, 2008), but outersurface c-type cytochromes (Holmes et al., 2006; Nevin
et al., 2009) are required to facilitate electron transfer
between the biofilm and the anode surface (Inoue et al.,
2010).
However,
current-consuming
fumarate-reducing
biofilms of Geobacter species are much thinner than
current-producing biofilms (Strycharz et al., 2008). Gene
expression patterns in current-consuming cells are very
different than those in current-producing cells and deletion of genes that are essential for current production do
not impact on current consumption and vice versa (Strycharz et al., 2010a). These results suggest that the routes
for electron transfer from electrodes to cells may be
different than they are for current production.
Electrobioremediation of metal and
organic contaminants
One of the most promising applications of direct electron
transfer from electrodes to microorganisms may be as a
strategy for bioremediation of contaminated environments. For example, microbial reduction of soluble U(VI)
to insoluble U(IV) has been proposed as a strategy for
immobilizing uranium in contaminated subsurface environments (Finneran et al., 2002; Anderson et al., 2003) or
for concentrating uranium after it is extracted from con-
taminated soils (Phillips et al., 1995). Geobacter sulfurreducens reduced U(VI) to U(IV) with an electrode serving
as the electrode donor (Gregory and Lovley, 2005). The
U(IV) adsorbed to the graphite electrode surface. Thus,
an advantage to supplying electrons with electrodes for
groundwater remediation is that the immobilized uranium
can be removed from the subsurface by intermittently
pulling up the electrodes and stripping off the uranium
with a simple extractant such as bicarbonate (Gregory
and Lovley, 2005). This in situ uranium bioremediation
approach contrasts with the more common practice of
adding organic electron donors to the groundwater which
can effectively promote U(VI) reduction, but the immobilized U(IV) remains in the subsurface, vulnerable to
potential reoxidation and release into the groundwater if
oxygen intrudes into the environment. Furthermore, supplying electrons with an electrode is expected to require
less maintenance, monitoring and energy than pumping
organic electron donors into the subsurface. As noted
above, electrons can be supplied from water with energy
derived from solar panels, making this form of remediation an attractive sustainable practice. A solar-powered
cathode has been deployed at a uranium-contaminated
field study site (K.H. Williams and D.R. Lovley, unpubl.
data), but large-scale deployment strategies have yet to
be described.
Another form of metal contamination amenable to
reductive precipitation is chromium because soluble,
highly toxic Cr(VI) is reduced to less soluble, less toxic
Cr(III). Cr(VI) was rapidly reduced in the cathode chamber
of a microbial fuel cell (Tandukar et al., 2009). Cr(VI)
reduction was dependent upon electrons supplied from
acetate oxidation at the anode and the presence of microorganisms in the cathode chamber. The 16S rRNA
sequences of the cathode community were analysed, and
sequences closely related to those of microorganisms
known to reduce Cr(VI) were recovered.
Chlorinated solvents are another prevalent class of
groundwater contaminants that are typically bioremediated with the addition of organic electron donors, which
may be fermented to provide hydrogen to dechlorinating
microorganisms (Loffler and Edwards, 2006). This is a
rather non-specific, inefficient process because it
also stimulates the growth of the non-dechlorinating,
hydrogen-producing fermentative microorganisms as well
as non-dechlorinating microorganisms, which compete for
the hydrogen. Abiotic electrochemical reduction of chlorinated solvents has proven impractical due to high costs
for metal catalysts, poor cathode stability and substantial
concomitant hydrogen production (Aulenta et al., 2008).
Direct electron transfer to dechlorinating microorganisms
may overcome many of these limitations because with
this approach it is possible to more specifically deliver
electrons to the dechlorinating microorganisms.
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology Reports, 3, 27–35
Feeding Microbes Electricity 31
Geobacter lovleyi reduced tetrachloroethene (PCE)
and trichloroethene (TCE) to cis-dichloroethene (cis-DCE)
with an electrode serving as a sole electron acceptor
(Strycharz et al., 2008). Delivering electrons to dechlorinating microorganisms in this manner may be particularly
useful for converting PCE to a soluble product near
source zones. Unlike PCE and TCE, which are resistant
to aerobic degradation, cis-DCE can be aerobically
degraded (Coleman et al., 2002). Therefore, electrodedriven reductive dechlorination of PCE and TCE to DCE in
an upgradient anaerobic zone, followed by aerobic degradation of DCE in an aerobic zone, with enhanced
oxygen production with a subsurface anode, is a possible
groundwater bioremediation strategy.
The possibility of more extensive reductive dechlorination was investigated with mixed cultures which contained
Dehalococcoides species expected to be capable of complete dechlorination to ethane (Aulenta et al., 2009a).
Additional dechlorination of DCE, with the production of
vinyl chloride and small of amounts of ethene, was
observed (Aulenta et al., 2007; 2009a). However, these
cultures required the presence of methyl viologen as an
electron shuttle. Methyl viologen is a highly toxic compound that is unlikely to be approved for use in groundwater and lacks long-term stability. Soluble methyl
viologen supported much higher rates of dechlorination
than methyl viologen adsorbed on the electrode. Another
mixed culture was developed which could dechlorinate
TCE without the addition of methyl viologen, but cis-DCE
accounted for over 80% of the dechlorination products (Aulenta et al., 2009b). Therefore, it remains to be
determined if there are organisms which can be enriched/
isolated that can directly accept electrons from an electrode for complete dechlorination of chlorinated
solvents.
Anaeromyxobacter dehalogenans reductively dehalogenated 2-chlorophenol to phenol with direct electron
transfer from an electrode serving as the sole electron
donor (Strycharz et al., 2010b). These results suggest
that chlorinated aromatics could be another target of
bioremediation with cathodes.
Reduction of perchlorate to chloride is an effective
method for removing this emerging groundwater contaminant (Coates and Achenbach, 2004). Providing electrons
with electrodes was considered to be a potentially beneficial strategy for the bioremediation of perchloratecontaminated waters because residual organic electron
donors used in more common treatment strategies cause
problems in subsequent water treatment steps (Thrash
et al., 2007). Previously described perchlorate-reducing
pure cultures required the electron shuttle anthraquinone2,6-disulfonate in order to promote electron transfer from
the electrode to the cells (Thrash et al., 2007). A strain
was enriched and isolated that could reduce perchlorate
without the need for an added shuttle, but it was considered that, under the conditions of reactor operation,
hydrogen was being produced at the cathode as an
electron carrier (Thrash et al., 2007).
A mixed culture was developed on a cathode surface
that reduced perchlorate with an electrode as the electron
donor without exogenously added electron shuttles
(Butler et al., 2010). The perchlorate-reducing community
had a composition that was significantly different than the
community that existed on the cathode when nitrate had
been provided as the electron acceptor. The electron
source for perchlorate reduction was the anode of a
microbial fuel cell. This demonstrated the potential for
perchlorate treatment with wastewater as the energy
source, but this application would be subject to the
limitations for large-scale treatment of wastewater with
microbial fuel cells described above.
Promoting nitrate reduction with electricity through the
electrolytic production of hydrogen has been studied
extensively because of the priority of removing nitrate in
wastewater treatment (Thrash and Coates, 2008). Direct
electron transfer from electrodes is beginning to receive
attention. Following the discovery that G. metallireducens
could reduce nitrate to nitrite with electrons derived from
an electrode (Gregory et al., 2004), several studies have
reported mixed cultures that could completely denitrify
nitrate with an electrode serving as the sole electron
donor (Park et al., 2005; Clauwaert et al., 2007a; Jia
et al., 2008; Virdis et al., 2008). The microorganisms
responsible for this process and their mechanisms of
interaction with cathodes warrant further study.
Oxygen reduction
Interest in microbial oxygen reduction at cathodes has
primarily been driven by the goal of developing more
effective, less expensive microbial fuel cells for the conversion of organic wastes to electricity. Abiotic electrochemical reduction of oxygen is often sluggish in the
absence of expensive metal catalysts, such as platinum.
This is major concern for power production with microbial
fuel cells (Clauwaert et al., 2007b; Rismani-Yazdi et al.,
2008). Early studies on microbial fuel cells harvesting
electricity from sediments noted an enrichment of microorganisms on cathodes distinct from those colonizing the
same graphite material, suspended in the aerobic water,
but not connected to an anode in the sediment (Holmes
et al., 2004). This suggested the possibility of a unique
microbial metabolism associated with the availability of
electrons at the cathode surface. The ability of mixed
communities that colonize cathodes in seawater to stimulate electron transfer at the cathode is now well documented (Bergel et al., 2005; Erable et al., 2010). Microbial
colonization of the carbon cathodes of microbial fuel cells
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology Reports, 3, 27–35
32 D. R. Lovley
can potentially lead to power production much higher than
sterile cathode controls and comparable to that with cathodes employing expensive metallic catalysts (Clauwaert
et al., 2007b; Rabaey et al., 2008; You et al., 2009). Electrochemical analyses indicated that the presence of
microorganisms on the cathodes significantly lowers the
cathodic charge transfer resistance (You et al., 2009).
A wide diversity of Gram-positive as well as Gramnegative microorganisms can promote oxygen reduction
at the cathode (Cordas et al., 2008; Rabaey et al., 2008;
Parot et al., 2009; Vandecandelaere et al., 2009; Cournet
et al., 2010; Erable et al., 2010). The mechanisms for
this are as yet unknown and a microorganism that can
conserve energy to support growth from oxygen reduction
with an electrode serving as the sole electron donor has
yet to be described. It is possible that oxygen reduction is
not linked to respiration as common cellular components,
including iron-containing enzymes such as catalase,
might catalyse a non-respiratory oxygen reduction
(Parot et al., 2009). Further research in this area seems
warranted because of the strong need for inexpensive
approaches to enhance the rate of cathode reactions
in microbial fuel cells in order to expand their range of
application.
Production of fuels and chemicals
One of the most exciting potential applications of powering microbial activity with electricity is microbial electrosynthesis, the process in which electricity serves as the
energy source for microbial reduction of carbon dioxide
into organic compounds (Nevin et al., 2010). Microbial
electrosynthesis offers the possibility of greatly increasing
the value of electrical energy that can be harvested with
renewable energy strategies such as solar and wind
because it is feasible to a produce a wide range of valuable chemical products that would otherwise need to be
synthesized from petroleum or biomass. The production
of liquid transportation fuels with microbial electrosynthesis is particularly attractive. This is because electricity
generation with renewable technologies is not continuous
or always synched with demand and it is difficult to store
electricity. Large-scale fuel production could readily
convert electrical energy into covalent carbon bonds permitting storage and delivery upon demand within existing
infrastructure (Nevin et al., 2010).
Microbial reduction of carbon dioxide with the release of
extracellular, multi-carbon products is the most preferable
form of microbial electrosynthesis because most desired
products will have more than one carbon, and extracellular release of products from cells attached to electrodes
simplifies product recovery. This form of microbial electrosynthesis is feasible with some acetogenic bacteria.
For example, the acetogen Sporomusa ovata formed bio-
films on graphite electrodes and could accept electrons
directly from the electrodes with the reduction of carbon
dioxide to acetate and small amounts of 2-oxobutyrate
(Nevin et al., 2010). Over 85% of the electrons consumed
in the system were recovered in these products. The
overall reaction of converting water and carbon dioxide to
organic products with the acetogens was the same as that
for photosynthesis, but with the significant difference that
the primary output was extracellular products rather than
biomass.
These results suggest that the reduction of carbon
dioxide with electrons derived directly from electrodes can
be an effective process for converting carbon dioxide to
extracellular, multi-carbon products. The fact that acetylCoA is an intermediate in acetate production in acetogens
suggests that it may be possible to engineer the production
of a wide diversity of products. For example, butanol is a
desirable transportation fuel and it has already been demonstrated that it is possible to express genes for butanol
production in the acetogen Clostridium ljungdahlii (Köpke
et al., 2010). Many other products are readily imagined.
If microbial electrosynthesis can be coupled with
photovolatics on a large scale, it offers the possibility of a
new form of photosynthesis that could have substantial
advantages over the traditional biomass-based approach
because: (i) photovolatics are orders of magnitude more
effective in capturing solar energy than biological photosynthesis, (ii) there is no need for high-quality land for
plant growth, (iii) microbial electrosynthesis is carried out
in closed systems eliminating the release of nutrient pollutants, and (iv) microbial electrosynthesis directly synthesizes products rather than biomass which requires further
processing, generating additional waste (Nevin et al.,
2010).
Another possibility is to use methanogenic microorganisms to reduce carbon dioxide to methane at the cathode
in a process termed electromethanogenesis (Cheng
et al., 2009). The possibility of driving methanogenesis
with electric current was first demonstrated with mixed
cultures, but required the electron shuttle mediator,
neutral red (Park et al., 1999). In subsequent studies
without mediator current capture efficiencies of 96% were
possible and methane could be produced under defined
conditions with a pure culture of Methanobacterium palustre (Cheng et al., 2009). Although this process was primarily discussed in terms of using the anode of a microbial
fuel cell as the electron source, electrons could be
obtained from water (Cheng et al., 2009). However,
efforts to replicate production of methane with M. palustre
in our laboratory have been unsuccessful (S. Hensley,
unpubl. data) and, in contrast to the initial report (Cheng
et al., 2009), there was substantial hydrogen production
at the cathode, consistent with a subsequent report
(Villano et al., 2010).
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology Reports, 3, 27–35
Feeding Microbes Electricity 33
Light-dependent carbon dioxide uptake, coupled with
current consumption observed with a mixed culture inoculum, was proposed as an alternative cathode reaction to
support organic matter oxidation in microbial fuel cells
(Cao et al., 2009). Presumably phototrophic microorganisms were using electrons derived from the cathode rather
than water for biomass production, but the alternative of
photosynthetic oxygen production followed by oxygen
reduction by the cathode was not conclusively eliminated.
Organic compounds may also serve as an electron
acceptor for electrons derived from electrodes. Electrodedriven reduction of fumarate to succinate has been
observed with G. sulfurreducens (Gregory et al., 2004;
Dumas et al., 2008). Mixed communities reduced acetate
to ethanol, but this required methyl viologen as an electron shuttle (Steinbusch et al., 2010). The vision of providing microorganisms with electrons via electron shuttles
to favourably influence fermentation towards the production of more desirable products or to transform organic
compounds into valuable drugs or chemicals (Park et al.,
1999) might also be feasible with direct electron transfer.
Hydrogen is another potential sustainable fuel that can
be produced electrochemically. Cathodic systems in
which microorganisms catalyse proton reduction to hydrogen could potentially be less expensive than platinumcatalysed abiotic systems and more stable than systems
that rely on hydrogenases (Rozendal et al., 2008). A
cathode biofilm was developed that produced hydrogen
eightfold faster than a control cathode poised at the same
potential (Rozendal et al., 2008). Addition of carbon
monoxide, an inhibitor of iron-hydrogenases, inhibited
hydrogen production, suggesting an enzymatic mode for
hydrogen production.
Hydrogen production with mixed culture systems can
be problematic due methanogens consuming hydrogen
(Clauwaert and Verstraete, 2009), thus defined systems
might be more effective. It seems likely that hydrogen
might be produced with existing pure cultures and direct
electron transfer from electrodes. For example, Geobacter species that are capable of accepting electrons
from electrodes (Gregory et al., 2004) are also capable of
hydrogen production (Cord-Ruwisch et al., 1998).
Future directions
It is now clear that some microorganisms can directly
accept electrons from electrodes and that direct electrode
to microbe electron transfer has a number of potential
applications. However, substantial engineering is required
in order to achieve envisioned applications. This will most
likely involve not only engineering the systems for delivering electrons, but in some instances will also require
genetic engineering of the organisms to promote desired
reactions. Enhancing the rates of electron transfer
between electrodes and microorganisms is a priority as is
the elucidation of the mechanisms for electron transfer
from electrodes to microorganisms. Electron transfer from
electrodes to cells may have natural analogues, such as
the microbial oxidation of reduced minerals (Thrash and
Coates, 2008), corrosion (Mehanna et al., 2009) and the
oxidation of reduced humic substances (Lovley et al.,
1999). However, as studies with microbial current production have shown (Lovley, 2008), microbial electronic
interaction with electrodes and natural materials can
have important differences. Thus, adaptive evolution with
selective pressure for microorganisms that accumulate
mutations favouring enhanced current consumption
may be a productive line of research, in a manner similar
to that observed with adaptive evolution for enhanced
current production (Yi et al., 2009). This approach has the
added benefit that genome resequencing of the improved
strains to identify beneficial mutations can provide insight
into the mechanisms for electronic interactions (Tremblay
et al., 2010). It is also important to determine the mechanisms by which microorganisms might conserve energy to
maintain cells and support growth when directly accepting
electrons from electrodes. Therefore, in the rush to
develop applications for electrode-driven microbial processes, hopefully there will also be the time and resources
for careful pure culture studies to develop a deep understanding of electron transfer from electrodes to microbes
in order to advance this field in a rational manner.
Acknowledgements
This work was supported by the Office of Science (BER)
U.S. Department of Energy Cooperative Agreement No.
DE-FC-02ER63446 and Agreement No. DE-AR0000087
from ARPA-E.
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