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A shift in the current: New applications and concepts formicrobe-electrode electron exchangeDerek R Lovley and Kelly P Nevin

Perceived applications of microbe-electrode interactions are

shifting from production of electric power to other

technologies, some of which even consume current.

Electrodes can serve as stable, long-term electron acceptors

for contaminant-degrading microbes to promote rapid

degradation of organic pollutants in anaerobic subsurface

environments. Solar and other forms of renewable electrical

energy can be used to provide electrons extracted from water

to microorganisms on electrodes at suitably low potentials for

a number of groundwater bioremediation applications as well

as for the production of fuels and other organic compounds

from carbon dioxide. The understanding of how

microorganisms exchange electrons with electrodes has

improved substantially and is expected to be helpful in

optimizing practical applications of microbe-electrode

interactions, as well as yielding insights into related natural

environmental phenomena.

Address

Department of Microbiology, University of Massachusetts, Amherst, MA

01003, United States

Corresponding author: Lovley, Derek R ([email protected])

Current Opinion in Biotechnology 2011, 22:1–8

This review comes from a themed issue on

Environmental biotechnology

Edited by Lindsay Eltis and Ariel Kushmaro

0958-1669/$ – see front matter

# 2011 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.copbio.2011.01.009

IntroductionElectrodes can supply electrons to support the respiration

of some microorganisms [1,2��] or can accept electrons,

serving as an electron acceptor to support anaerobic

oxidation of organic compounds or inorganic electron

donors such as hydrogen and elemental sulfur [3,4��].Electron flow between microorganisms and electrodes in

both directions is of significance, not only because these

are interesting forms of microbial respiration, which may

provide insights into how microorganisms may function in

natural environments, but also because the ability of

microorganisms to consume or produce electrical current

has potential practical applications in the environmental

and bioenergy fields.

Please cite this article in press as: Lovley DR, Nevin KP. A shift in the current: New applications an

j.copbio.2011.01.009

www.sciencedirect.com

Although there has been intense focus on producing elec-

trical power with microbial fuel cells over the last decade,

some of the early optimism for power production has

waned and there is now a major shift in focus to other

applications. After hundreds of studies, it is apparent that

just about any form of organic matter that microbes can

degrade can be converted to current [4��] and powering

electronic equipment with electricity harvested from the

complex organic matter in aquatic sediments with benthic

microbial fuel cells continues to be a promising application

[5–8]. However, after some of the rather obvious design

flaws in early microbial fuel cells were rectified, there has

been little increase in the power output of microbial fuel

cells in recent years [9]. Furthermore, effectively scaling

microbial fuel cells to sizes that can handle large volumes of

organic waste may be problematic [10��]. Economic assess-

ments indicate that even if the current density and scaling

issues can be resolved, current harvesting will probably

need to be supplemented with some value-added reaction

for the treatment of wastewaters with microbial fuel cell

technology to be competitive with other, more mature

technologies [11��,12]. One strategy may be to add elec-

trical energy to the wastewater treatment system to over-

come electrochemical limitations and focus on product

formation [13]. In addition to the well-known possibility

of producing hydrogen at the cathode [14��], it has been

suggested that is also feasible to generate peroxide [15] or

caustic [16] through abiotic processes at the cathode. Water

desalination may also be feasible with energy derived from

wastewater in a novel microbial fuel cell design [17].

However, until solutions for increasing power output

and scaling are conceived, wastewater-related processes

may be one of the less attractive applications of microbe-

electrode interactions. Therefore, this review focuses on

other technologies in which microbe-electrode interactions

might be employed.

Many of the most promising applications for microbe-

electrode interactions are based on directly supplying

electrons to microorganisms at a cathode to permit them

to catalyze useful processes. It is possible to indirectly

transfer electrons from electrodes to microorganisms via

the production of hydrogen gas or the reduction of electron

shuttle molecules, but as previously reviewed [1,18], these

indirect approaches have serious limitations in practical

application and will not be discussed in detail here.

A major conceptual shift in such studies is to move away

from linking cathode processes to the oxidation of organic

matter in wastewater at the anode as the source of

d concepts for microbe-electrode electron exchange, Curr Opin Biotechnol (2011), doi:10.1016/


http://dx.doi.org/10.1016/j.copbio.2011.01.009


mailto:[email protected]


2 Environmental biotechnology


Figure 1

Sediment-Water Interface

OrganicContaminants

Adsorption andConcentration ofContaminants onAnode

Cells Co-Localized withContaminants andElectron Acceptor

OrganicContaminants

CO2

O2 2H2O

Current Opinion in Biotechnology

Strategy for stimulating the anaerobic oxidation of organic contaminants

in sediments.

electrons. Although such anodes can supply electrons at a

low potential and thus lower the energetic costs of sup-

plying electrons to the cathode [14��], wastewater anodes

tie processes to the wastewater treatment concept. In

addition to practical concerns about scaling, wastewater

treatment plants will often not be located near sites where

they are required for applications such as groundwater

bioremediation. Water is abundant and ubiquitous, mak-

ing it an ideal electron donor for many perceived cathode

applications [1].

There have also been recent conceptual shifts in models

for microbe-electrode interactions that may impact on

strategies for the optimization of proposed microbe-elec-

trode technologies. The purpose of this review is to

update progress since a similar recent review [19], with

a focus on new applications and microbial physiology.

Non-microbiological aspects, such as reactor design and

materials, or descriptive studies documenting the com-

position of microbial communities colonizing electrodes

are not reviewed here.

Beyond power production: novel applicationsof microbe-electrode exchangeMicrobe-electrode systems designed for wastewater

treatment have to compete with mature, proven technol-

ogies, and require large capital investments. However,

there are other applications for microbial fuel cell tech-

nology where the competition may not be as intense,

especially when generation of electric power is not the

goal.

One area ripe for application is bioremediation of aquatic

sediments and groundwater. For example, inexpensive

but durable graphite electrodes deployed in sediments

not only serve as a low-maintenance, long-lived, desir-

able electron acceptor for anaerobic respiration, but also

can adsorb contaminants from the surrounding sediment,

co-localizing the contaminants, contaminant-degrading

microorganisms, and an electron acceptor in the same

location (Figure 1). This possibility of accelerating

anaerobic oxidation of organic contaminants in this man-

ner was first proposed back in 2002 (as reviewed in [20])

and has now been demonstrated for aromatic hydrocar-

bons [20], 1,2-dichloroethane [21], pyridine [22], phenol

[23], and possibly alkanes [24]. It seems likely that any

organic contaminants that microbes have been shown to

anaerobically oxidize with other electron acceptors can

be oxidized with electron transfer to an electrode.

Although it has been suggested that salt bridges would

need to be introduced into the subsurface to promote

proton flux between the anode and cathode for subsur-

face bioremediation with this technology [25], this is

unlikely [26�].

Electrodes deployed in anoxic subsurface environments

might also make it feasible to monitor microbial activity


j.copbio.2011.01.009


in groundwater in real time [26�]. As has previously been

observed in many other environments, Geobacter species

readily colonized graphite electrodes deployed in the

subsurface of a uranium-contaminated aquifer, producing

current levels that corresponded with the availability of

acetate added to the groundwater to promote U(VI)

reduction. This approach could be useful for monitoring

microbial activity in a diversity of environments, in-

cluding other planets [27].

Electron transfer from electrodes to cells may also have

bioremediation applications. Providing electrons to

microorganisms with electrodes shows substantial

promise as a strategy for bioremediation of groundwater

contaminated with metals or chlorinated solvents

(Figure 2). Geobacter-mediated cathode-driven bioreme-

diation of uranium-contaminated groundwater via reduc-

tive precipitation may be more effective, simpler, and less

expensive than the more familiar approach of enhancing

the activity of metal-reducing microorganisms with the

addition of organic compounds [1]. Other metal contami-

nants, such as Cr(VI), might be bioremediated in a similar

manner [28,29]. Promoting reductive dechlorination with

electrodes as the electron source [30–34] also has signifi-

cant potential advantages, but it seems important that this

be achieved with direct electron transfer to the dechlor-

inating microorganisms, rather than promoting electron

transfer with toxic electron shuttles or generating hydro-

gen at the cathode as has been done in some studies.

Other contaminants such as perchlorate [35] or nitrate

[36] may also be removed via reduction at the cathode.

Although the treatment of these contaminants was dis-

cussed in terms of wastewater treatment, these current-





A shift in the current: New applications and concepts for microbe-electrode electron exchange Lovley and Nevin 3


Figure 2

PowerSupply

PCE

PCE PCE

DCE

DCE DCEDCE

DCE

DCE

PCE

DCE

GW flow

Cathode

Anode

O2 CO2

H2O

e-


ContaminantSource Zone

Strategy for sequentially stimulating reductive dechlorination and aerobic degradation of partially dechlorinated products in the subsurface with solar

power.

driven microbial reduction may also be a viable ground-

water bioremediation strategy. Electrodes offer the

possibility of supplying electrons for bioremediation in

very specific locations and effectively co-localizing the

electron donor and the appropriate organisms, offering

the possibility of pre-colonizing the electrodes with the

desired organisms. The possibility of using solar technol-

ogy to sustainably generate the electricity necessary to

supply the electrons for such groundwater bioremediation

efforts is particularly attractive [32].

Increasing reliance on solar energy as a renewable source

of electricity is the major impetus for another cathode-

driven application, termed microbial electrosynthesis

(Box 1). Acetogenic microorganisms, which naturally

reduce carbon dioxide with hydrogen as the electron

donor to produce acetate as an endproduct, can substitute

an electrode as the electron donor for carbon dioxide

reduction, producing primarily acetate and small amounts

of other organic acids and alcohols (Nevin KP, Hensley

SA, Franks AE, Summers ZM, Ou J, Woodard TL,

Snoeyenbo-West OL, Lovley DR: Electrosynthesis of

organic compounds from carbon dioxide catalyzed by a

diversity of acetogenic microorganisms, unpublished


j.copbio.2011.01.009


data) [37]. Recovery of electrons consumed in products

was high (ca. 85%) and ca. 70% of the electrical energy

expended was recovered in products. The cathode bio-

films of acetogens maintained sustained activity and

viability on the electrodes for months, without forming

thick biofilms, suggesting that the microbes gain small

amounts of energy from the reduction of carbon dioxide.

Acetyl-CoA, the central intermediate in acetate pro-

duction in acetogens, is the building block for microbial

synthesis of a wide diversity of desirable organic products

[38] and it has been demonstrated that it should be

possible with genetic engineering to divert carbon and

electron flow in acetogenic microbes toward the pro-

duction of butanol [39��], a fuel that can be transported

through existing pipelines and burned in automobile

engines without modification. Thus, microbial electro-

synthesis offers the possibility of converting renewable

but intermittent forms of energy, such as solar and wind,

into liquid transportation fuels or desirable chemicals

much more efficiently and with less potential environ-

mental degradation than biomass-based strategies (Box

1). It would be conceivable to use microbial electrosynth-

esis as a carbon sequestration process, producing organic

compounds that are resistant to degradation for long-term







Box 1 Microbial electrosynthesis: artificial photosynthesis for

direct production of fuels

Electrosynthesis of organic compounds via abiotic or enzymatic

catalysis of carbon dioxide reduction at electrode surfaces has been

evaluated as a strategy for converting electricity into useful organic

products for some time [77,78]. Microbial catalysts might be better.

They are inexpensive to grow and, if the microbes catalyzing the

reactions gain enough energy for cell maintenance, are self-

sustaining and long-lived.

Microbial electrosynthesis can be powered with any source of

electricity, but when solar power is utilized the overall reaction

(CO2 + H2O! organic compounds + O2) powered by light is the

same as photosynthesis. However, microbial electrosynthesis is

ca. 100-fold more efficient than plants in converting solar energy

into organic compounds and can produce desired products

directly whereas producing fuels from biomass requires additional

energy inputs and only a fraction of the energy in the biomass is

recovered as fuel. Microbial electrosynthesis also does not require

arable land; the large quantities of water required for growing

biomass and then processing biomass to fuel; and can avoid the

environmental degradation associated with large-scale biomass

production. Thus, microbial electrosynthesis could transform the

bioenergy field because it offers the possibility of converting

renewable, but intermittent, sources of electricity into fuels or other

desirable organic compounds that are energy dense and can

readily be stored, distributed, and utilized within the existing

infrastructure [1,37].

carbon removal. However, the study of microbial electro-

synthesis is in its infancy and significant engineering of

the microbes and the reactors are required for practical

application.

It was suggested that some methanogens could also

directly accept electrons from electrodes, catalyzing the

reduction of carbon dioxide to methane [40], but sub-

sequent studies have questioned whether hydrogen pro-

duced at the cathode was the actual electron donor [1,41]

because hydrogen is typically produced at the low poten-

tials that were required for active methanogenesis. Micro-

organisms accepting electrons from cathodes may

catalyze proton reduction to hydrogen gas with hydro-

genases [14��,42,43]. Pure cultures that are capable of

reducing protons with electrons derived from electrodes

have not yet been described, but such organisms could

eliminate the need for expensive platinum catalysts for

hydrogen production.

Microorganisms can promote electron transfer to oxygen

on cathodes [1,2��]. This may not be linked to aerobic

respiration [44,45], but rather the result of interaction of

oxygen with a diversity of reduced cell components.

There is often an enrichment of specific microorganisms

on the cathodes of microbial fuel cells deployed in open

environments, and thus it is not clear whether preemptive

colonization of cathodes with microorganisms highly

effective in catalyzing oxygen reduction would improve

the long-term kinetics of oxygen reduction in microbial

fuel cells for most practical applications.


j.copbio.2011.01.009


Mechanisms for microbe-electrode electronexchangeOptimization of any of the applications discussed above, as

well as conceptualization of novel applications, will prob-

ably profit from an understanding of how microorganisms

exchange electrons with the electrode surface. The dis-

cussion here will be limited to mechanistic studies with

defined pure cultures for which the results are more readily

interpreted. Pure culture studies have primarily focused on

Geobacter species, chosen because they are often the pre-

dominant organisms that naturally colonize high current

density anodes in a diversity of environments, or Shewanellaspecies, which are rarely found as anode inhabitants, but

many consider easier to cultivate in the laboratory because

they can also use oxygen as an electron acceptor.

Geobacter sulfurreducens has been intensively studied

because it is often cited as the species most closely related

to those Geobacter species that predominate on anodes and

because it produces the highest current density of any

known pure culture [46,47]. Electrochemical studies [48–50] have confirmed multiple lines of earlier research [51]

that soluble electron shuttles are not important for elec-

tron transfer from G. sulfurreducens to anodes. Despite this,

cells at the outer edge of the relatively thick (>50 mm)

anode biofilms of G. sulfurreducens appear to be metabo-

lically active [52] as are cells near the anode surface, even

though they generate relatively low pH [53]. Microarray

analysis of gene expression and gene deletion studies

suggest that the electrically conductive pili and the c-type

cytochrome OmcZ are essential for optimal current pro-

duction [54]. Adaptive evolution studies in which there

was strong selective pressure for enhanced current pro-

duction yielded a hyperpiliated strain [46]. Characteriz-

ation of OmcZ demonstrated that it contained eight

hemes with potentials ranging from �420 to �60 mV

[55]. Localization of OmcZ with gold-labeled antibodies

and transmission electron microscopy revealed that

OmcZ was not closely associated with cells and accumu-

lated near the anode surface [56]. This is consistent with

the prediction of increased c-type cytochromes at the

biofilm-electrode interface [57,58]. These findings,

coupled with electrochemical analyses [49], suggest that

OmcZ functions as an ‘electrochemical gate’ to promote

electron transfer onto the electrode [56]. This model

(Figure 3a) of long-range electron conduction via pili

and then electron transfer onto the electrode via OmcZ,

is similar to the model for Fe(III) oxide reduction

(Figure 3b), in which electrons are conducted away from

the cell via pili and then electrical contact between pili

and Fe(III) oxide is facilitated by the c-type cytochrome

OmcS, which is localized along the pili [59�]. In both

instances, long-range extracellular transfer is along pili

and c-type cytochromes are required to promote the final

transfer to the insoluble electron acceptor. The pathway

for electron transfer from the inner membrane to the

outer cell surface during electron transfer to electrodes is







Figure 3

(a) (b)

(c)

Pilin-MediatedConductionThroughBiofilm

OmcZ-MediatedElectron Transfer fromBiofilm to Anode

Electron Transfer Along Pili with OmcS-Mediated Electron Transfer to Fe(III) Oxide

OxidizedFlavin

ReducedFlavin

ElectrodeorFe(III) Oxide


Models for the predominant mechanisms for electron transfer to electrodes (a) and Fe(III) oxides (b) by Geobacter sulfurreducens and electron transfer

to electrodes and Fe(III) oxides by Shewanella oneidensis (c).

considered to involve a series of periplasmic and outer-

membrane c-type cytochromes. The abundant c-type

cytochromes also appear to act as capacitors to store

electrons when electron transfer is impeded [58,60�], as

previously proposed [61]. Other redox-active proteins

such as multi-copper proteins may also be important in

the electron transfer [62]. Electrochemical analysis

suggests that the final electron transfer from Geobacterbiofilms to the anode is fast enough to permit cells in the

biofilm to respire as fast as they can with soluble Fe(III) as

the electron acceptor [60�], suggesting that engineering

Geobacter to respire faster [63], or to pack more cells into

the biofilm, could result in higher current densities.

The current model for extracellular electron transfer in

Shewanella oneidensis is significantly different (Figure 3c).

Electron transfer to electrodes does not require direct

contact [64,65] as had previously been demonstrated for

Fe(III) oxides, and although S. oneidensis also has con-

ductive pili [66], they are not required for electron trans-

fer to Fe(III) or electrodes [67��]. The primary outer-

surface c-type cytochromes required for reduction of

Fe(III) and electrodes appear to be associated with the

cell surface, not pili [68] and although they may be able to

poorly transfer electrons to insoluble electron acceptors,

the primary role of the cytochromes appears to be the


j.copbio.2011.01.009


reduction of flavins which are released from the cell and

serve as an electron shuttle for Fe(III) and electrode

reduction [69,70��,71,72��].

Electron transfer from electrodes to microbes may not be

a simple reversal of electron transfer from cells to elec-

trodes. Current-consuming biofilms of G. sulfurreducenshad much lower expression of genes for pili and OmcZ,

which are essential for optimal current production, than

current-producing biofilms and deletion of the genes for

pili or OmcZ production had no impact on the capacity for

current uptake [73]. One of the most highly up-regulated

genes in current-consuming biofilms was a gene for a

putative, mono-heme c-type cytochrome predicted to be

located in the periplasm [73]. Deleting the gene for this

cytochrome had no impact on the capacity for current

production, but completely inhibited the ability of cells to

accept electrons from electrodes [73].

ConclusionsAs the understanding of microbe-electrode electron

exchange improves, it is becoming apparent that producing

electric current may not be the most important, short-term,

practical application of this phenomenon. In fact, some of

the most promising microbe-electrode technologies may

require aninput ofelectricalpower. Additionalapplications,







not only in environmental biotechnology and bioenergy,

but also in other fields, are likely to continue to emerge.

Furthermore, understanding how microorganisms electro-

nically interact with electrodes may provide important

insights into how microorganisms may electronically inter-

act with conductive materials [74�] or other cells [75] in

natural environments, which should be helpful in under-

standing interesting phenomena, such as apparent rapid

electron transfer through marine sediments [76�]. Thus, for

both natural science and practical applications, a basic un-

derstanding of how cells exchange electrons with materials

outside the cell is essential.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

�� of outstanding interest

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2.��

Rosenbaum M, Aulenta F, Villano M, Angenent LT: Cathodes aselectron donors for microbial metabolism: which extracellularelectron transfer mechanisms are involved? BioresourceTechnol 2010 doi: 10.1016/j.biortech.2010.07.008.

Thought-provoking speculation on the potential mechanisms for electrontransfer from cathodes to microbes.

3. Lovley DR, Nevin KP: Electricity production with electricigens.In Bioenergy. Edited by Wall JD, Harwood CS, Demain AL. ASMPress; 2008:295-306.

4.��

Pant D, Van Bogaert G, Diels L, Vanbroekhoven K: A review ofsubstrates use in microbial fuel cells (MFCs) for sustainableenergy production. Bioresource Technol 2010, 101:1533-1543.

Excellent summary of the range of electron donors that can be oxidized inmicrobial fuel cells.

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Demonstration that microbial fuel cells do not scale in a linear manner.

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Foley JM, Rozendal RA, Hertle CK, Lant PA, Rabaey K: Life cycleassessment of a high-rate anaerobic treatment, microbial fuelcells and microbial electrolysis cells. Environ Sci Technol 2010,44:3629-3637.

Insights into the economic realities of wastewater treatment with micro-bial fuel cell technology.

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Williams KN, Nevin KP, Franks AE, Englert A, Long PE, Lovley DR:Electrode-based approach for monitoring in situ microbialactivity during subsurface bioremediation. Environ Sci Technol2010, 44:47-54.

Demonstration that current can be produced with long-range separationof anode and cathode in the subsurface and introduction of a newconcept for estimating rates of microbial metabolism in the subsurface.

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33. Strycharz SM, Gannon SM, Boles AR, Nevin KP, Franks AE,Lovley DR: Anaeromyxobacter dehalogens interacts with apoised graphite electrode for reductive dechlorination of 2-chlorophenol. Environ Microbiol Rep 2010:289-294.

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Demonstrates the promise of whole-genome sequencing and geneticmanipulation for novel bioenergy strategies with acetogenic bacteria.

40. Cheng S, Xing D, Call DF, Logan BE: Direct biological conversionof electrical current into methane by electromethanogenesis.Environ Sci Technol 2009, 43:3953-3958.

41. Villano M, Aulenta F, Ciucci C, Ferri T, Giuliano A, Majone M:Bioelectrochemical reduction of CO2 to CH4 via direct andindirect extracellular electron transfer by a hydrogenophilicmethanogenicculture.BioresourceTechnol2010,101:3085-3090.

42. Rozendal RA, Jeremiasse AW, Hamelers HVM, Buisman CJN:Hydrogen production with a microbial biocathode. Environ SciTechnol 2008, 42:629-634.

43. Jeremiasse AW, Hamelers HVM, Buisman CJN: Microbialelectrolysis cell with a microbial biocathode.Bioelectrochemistry 2010, 78:39-43.

44. Parot S, Nercessian O, Delia M-L, Achouak W, Bergel A:Electrochemical checking of aerobic isolates fromelectrochemically active biofilms formed in compost. J ApplMicrobiol 2009, 106:1350-1390.

45. Freguia S, Tsujimura S, Kano K: Electron transfer pathwaysin microbial oxygen biocathodes. Electrochim Acta 2010,55:813-818.

46. Yi H, Nevin KP, Kim B-C, Franks AE, Klimes A, Tender LM,Lovley DR: Selection of a variant of Geobacter sulfurreducenswith enhanced capacity for current production in microbialfuel cells. Biosens Bioelectron 2009, 24:3498-3503.

47. Nevin KP, Richter H, Covalla SF, Johnson JP, Woodard TL, Jia H,Zhang M, Lovley DR: Power output and columbic efficienciesfrom biofilms of Geobacter sulfurreducens comparable tomixed community microbial fuel cells. Environ Microbiol 2008,10:2505-2514.

48. Marsili E, Baron DB, Shikhare I, Coursolle D, Gralnick JA, Bond DR:Shewanella secretes flavins that mediate extracellularelectron transfer. PNAS 2008, 105:3968-3973.

49. Richter H, Nevin KP, Jia H, Lowy DA, Lovley DR, Tender LM:Cyclic voltammetry of biofilms of wild type and mutantGeobacter sulfurreducens on fuel cell anodes indicatespossible roles of OmcB, OmcZ, type IV pili, and protons


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in extracellular electron transfer. Energy Environ Sci 2009,2:506-516.

50. Marsili E, Rollefson JB, Baron DB, Hozalski RM, Bond DR:Microbial biofilm voltammetry: direct electrochemicalcharacterization of catalytic electrode-attached biofilms. ApplEnviron Microbiol 2008, 74:7329-7337.

51. Lovley DR: Extracellular electron transfer: wires, capacitors,iron lungs, and more. Geobiology 2008, 6:225-231.

52. Franks AE, Nevin KP, Glaven RH, Lovley DR: Microtomingcoupled with microarray analysis to evaluate potentialdifferences in the metabolic status of Geobactersulfurreducens at different depths in anode biofilms. ISME J2010, 4:509-519.

53. Franks AE, Nevin KP, Jia H, Izallalen M, Woodard TL, Lovley DR:Novel strategy for three-dimensional real-time imaging ofmicrobial fuel cell communities: monitoring the inihibtoryeffects of proton accumulation within the anode biofilm.Energy Environ Sci 2009, 2:113-119.

54. Nevin KP, Kim B-C, Glaven RH, Johnson JP, Woodard TL,Methe BA, DiDonato RJ Jr, Covalla SF, Franks AE, Liu A et al.:Anode biofilm transcriptomics reveals outer surfacecomponents essential for high currency power production inGeobacter sulfurreducens fuel cells. PLoS ONE 2009, 4:e5628.

55. Inoue K, Qian X, Morgado L, Kim B-C, Mester T, Izallalen M,Salgueiro CA, Lovley DR: Purification and characterization ofOmcZ an outer-surface, octaheme, c-type cytochromeessential for optimal current production by Geobactersulfurreducens. Appl Environ Microbiol 2010, 76:3999-4007.

56. Inoue K, Leang C, Franks AE, Woodard TL, Nevin KP, Lovley DR:Specific localization of the c-type cytochrome OmcZ at theanode surface in current-producing biofilms of Geobactersulfurreducens. Environ Microbiol Rep 2010. 10.1111/j.1758-2229.2010.00210.x.

57. Busalmen JP, Esteve-Nunez A, Berna A, Feliu JM: C-typecytochromes wire electricity-producing bacteria toelectrodes. Angnew Chem Int Ed 2008, 47:4874-4877.

58. Busalmen JP, Esteve-Nunez A, Berna A, Feliu JM: ATR-SEIRAscharacterization of surface redox processes in G.sulfurreducens. Bioelectrochemistry 2010, 78:25-29.

59.�

Leang C, Qian X, Mester T, Lovley DR: Alignment of the c-typecytochrome OmcS along pili of Geobacter sulfurreducens.Appl Environ Microbiol 2010, 76:4080-4084.

New model for coupling electron flow through pili and cytochromes forextracellular electron transfer.

60.�

Marsili E, Sun J, Bond DR: Voltammetry and growth physiologyof Geobacter sulfurreducens biofilms as a function ofgrowth stage and imposed potential. Electroanalysis 2010,22:865-874.

In depth analysis of electron transfer through Geobacter sulfurrreducensanode biofilms identifying the key aspects of this process.

61. Esteve-Nunez A, Sosnik J, Visconti P, Lovley DR:Fluorescent properties of c-type cytochromes revealtheir potential role as an extracytoplasmic electronsink in Geobacter sulfurreducens. Environ Microbiol 2008,10:497-505.

62. Holmes DE, Mester T, O’Neil RA, Larrahondo MJ, Adams LA,Glaven R, Sharma ML, Ward JA, Nevin KP, Lovley DR: Genes fortwo multicopper proteins required for Fe(III) oxide reduction inGeobacter sulfurreducens have different expression patternsboth in the subsurface and on energy-harvesting electrodes.Microbiology 2008, 145:1422-1435.

63. Izallalen M, Mahadevan R, Burgard A, Postier B, DiDonato R,Sun J, Schilling CH, Lovley DR: Geobacter sulfurreducens strainengineered for increased rates of respiration. Metabolic Eng2008, 10:267-275.

64. Lanthier M, Gregory KB, Lovley DR: Electron transfer toelectrodes with high planktonic biomass in Shewanellaoneidensis fuel cells. FEMS Microbiol Lett 2008, 278:29-35.

65. Jiang X, Hu J, Fitzgerald LA, Biffinger JC, Xie P, Ringeisen BR,Lieber CM: Probing electron transfer mechanisms in



http://dx.doi.org/10.1128/mBio.00103-00110





Shewanella oneidensis MR-1 using a nanoelectrode platformand single-cell imaging. Proc Natl Acad Sci USA 2010 http://www.pnas.org/cgi/doi/10.1073/pnas.1011699107.

66. El-Naggar MY, Gorby YA, Xia W, Nealson KH: The moleculardensity states in bacterial nanowires. Biophys J 2008,95:L10-L12.

67.��

Bouhenni RA, Vora GJ, Biffinger JC, Shirodkar S, Brockman K,Ray R, Wu P, Johnson BJ, Biddle EM, Marshall MJ et al.:The role of Shewanella oneidensis MR-1 outer surfacestructures in extracellular electron transfer. Electroanalysis2010, 22:856-864.

Important study using genetic approach to rigorously test several modelsfor extracellular electron transfer.

68. Shi L, Richardson DJ, Wang Z, Kerisit SN, Rosso KM, Zachara JM,Fredrickson JK: The roles of outer membrane cytochromes ofShewanella and Geobacter in extracellular electron transfer.Environ Microbiol Rep 2009, 1:220-227.

69. Peng L, You S-J, Wang J-Y: Electrode potential regulatescytochrome accumulation on Shewanella oneidensis cellsurface and the consequence to bioelectrocatalytic currentgeneration. Biosens Bioelectron 2010, 25:2530-2533.

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Ross DE, Brantley SL, Tien M: Kinectic characterization ofOmcA and MtrC, terminal reductases involved in respiratoryelectron transfer for dissimilatory iron reduction inShewanella oneidensis MR-1. Appl Environ Microbiol 2009,75:5218-5226.

Demonstrates likely in vivo role of outer surface cytochromes in aquantitative manner.

71. Coursolle D, Baron DB, Bond DR, Gralnick JA: The Mtr respiratorypathway is essential for reducing flavins and electrodes inShewanella oneidensis. J Bacteriol 2010, 192:467-474.

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Baron DB, LaBelle E, Coursolle D, Gralnick JA, Bond DR:Electrochemical measurements of electron transfer


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kinetics by Shewanella oneidensis MR-1. J Biol Chem 2009,284:28865-28873.

Just one of a series of studies by the Minnesota team that has eloquentlydemonstrated the power of combining electrochemical and more tradi-tional physiological studies to elucidate extracellular electron transfermechanisms.

73. Strycharz SM, Glaven RH, Coppi MV, Gannon SM, Perpetua LA,Liu A, Nevin KP, Lovley DR: Gene expression and deletionanalysis of mechanisms for electron transfer fromelectrodes to Geobacter sulfurreducens. Bioelectrochemistry2010 doi: 10.1016/j.bioelechem.2010.07.005.

74.�

Kato S, Nakamura R, Kai F, Wantanabe K, Hashimoto K:Respiratory interactions of soil bacteria with(semi)conductive iron-oxide minerals. Environ Microbiol 2010doi: 10.1111/j.1462-2920.2010.02284.x.

Novel concept for electron transfer in sedimentary environments.

75. Summers ZM, Fogarty H, Leang C, Franks AE, Malvankar NS,Lovley DR: Direct exchange of electrons within aggregates ofan evolved syntrophic co-culture of anaerobic bacteria.Science 2010, 330:1413-1415.

76.�

Nielsen LP, Risgaard-Petersen N, Fossing H, Christensen PB,Sayama M: Electric currents couple spatially separatedbiogeochemical processes in marine sediment. Nature 2010,463:1071-1074.

Surprising finding of apparent rapid long-range electron conductionthrough marine sediments.

77. Cole EB, Bocarsly AB: Photochemical, electrochemical, andphotochemical reduction of carbon dioxide. In Carbon Dioxideas Chemical Feedstock. Edited by Aresta M.. Wiley-VCH VerlagGmbH & Co; 2010:291-316.

78. Centi G, Perathoner S: Opportunities and prospects in thechemical recycling of carbon dioxide to fuels. Catal Today2009, 148:191-205.



http://www.pnas.org/cgi/doi/10.1073/pnas.1011699107

http://www.pnas.org/cgi/doi/10.1073/pnas.1011699107

http://dx.doi.org/10.1016/j.bioelechem.2010.07.005

http://dx.doi.org/10.1111/j.1462-2920.2010.02284.x



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