Electrochemical gradients are the backbone of basic cellular functions, including chemo-osmotic transport and ATP synthesis. Microbial growth, terminal respiratory proteins and external electron transfer are major pathways competing for electrons. In BESs (bioelectrochemical systems), such as MFCs (microbial fuel cells), the electron flow can be via soluble inorganic/organic molecules or to a solid surface. The flow of electrons towards a solid surface can be via outer-membrane cytochromes or electron-shuttle molecules, mediated by conductive protein nanowires or extracellular matrices. In MECs (microbial electrolysis cells), the anode potential can vary over a wide range, which alters the thermodynamic energy available for bacteria capable of donating electrons to the electrode [termed EAB (electroactive bacteria)]. Thus the anode potential is an important electrochemical parameter determining the growth, electron distribution/transfer and electrical activity of films of these bacteria on electrodes. Different optimal applied potentials to anodes have been suggested in the literature, for selection for microbial growth, diversity and performance in biofilms on electrodes. In the present paper, we review the effects of anode potentials on electron-transfer properties of such biofilms, and report on the effect that electrochemical cell configuration may have on performance.

Microbial respiration and electron exchange

Electron-transfer reactions are fundamental to metabolism and there are emerging views on how micro-organisms exchange electrons with extracellular donors or acceptors. Microbes thrive on the energy they gain and conserve energy by ‘moving’ electrons from low-potential electron donors (e.g. reduced organic and inorganic molecules) to higher-potential electron acceptors (e.g. oxidized organic and inorganic molecules). Many donors and acceptors are freely diffusible gases or soluble species that are easily transported and metabolized within living cells. Some others (e.g. those being too large or insoluble to enter the cell) are oxidized/reduced at the exterior of the cell. For the task of exchanging electrons with extracellular donors or acceptors, it has been suggested that bacteria employ a number of strategies, ranging from the use of electron-transfer proteins located on the OM (outer membrane) (e.g. cytochromes), soluble redox shuttles (e.g. pyocyanin) or conduction through the ECM (extracellular matrix) by microbial appendages (e.g. nanowires) or redox self-exchange [15], to the establishment of a syntrophic relationship with other micro-organisms via interspecies or intraspecies electron transfer.

Direct electron transfer between microbes and minerals [such as iron and manganese (hydro)oxides] is a widely studied interaction for extracellular anaerobic respiration. For example, in aquatic–terrestrial interfaces, degradation of naturally occurring organic matter is coupled with reduction of solid-phase oxide mineral oxides (iron or manganese) [6]. Indirect electron transfer can also occur via small molecules such as metal chelates operating as electron shuttles [7]. Recently, Nielsen et al. [8] reported that natural electric currents driven by bacterial extracellular electron-transfer processes run through marine sediments and couple biogeochemical processes (redox reactions) in widely spatially separated layers of marine sediments, such as sulfide oxidation in the lower sediment layers with oxygen reduction in the upper layers.

Extracellular electron transfer and bioelectrochemical systems

A long time before some of the fundamental aspects of EET (extracellular electron transfer) mechanisms were delineated, at both a cellular and a genetic level, researchers had reported that microbial degradation of organic matter could generate an electric current, experimentally measurable with electrodes [9]. More recently, Kim et al. [10] reported on a fuel-cell-type biosensor for lactate using electron transfer to electrodes by a dissimilatory metal-reducing bacterium, Shewanella putrefaciens IR-1. Under the operational conditions, the bacterial cell suspension generated current without the addition of an exogenous redox mediator, in the presence of lactate. It is only relatively recently that solid-state electrodes (e.g. graphite-based materials) have been used to mimic and replace naturally occurring extracellular electron donors and acceptors [1] to produce BESs (bioelectrochemical systems). Systematic investigations of the microbial communities enriched in BESs revealed the presence of many different bacteria, not only the dissimilatory metal-reducers, as had been initially speculated. This finding suggests that reasons other than respiration and energy yield using solid metal oxides as electron acceptors are behind the capacity of micro-organisms to carry out EET. These biochemical pathways may include the establishment of syntrophic relationships via interspecies electron transfer, where electrons are transferred instead of chemical species, or even cell–cell communication via soluble (or cell or pilus-attached or ECM-embedded) electron-shuttling molecules [4,5,11,12].

The capacity of bacteria to drive oxidation and reduction reactions at solid-state electrodes can be exploited to provide a plethora of BES-based applications, such as MFCs (microbial fuel cells) and MECs (microbial electrolysis cells) [collectively called MXCs (microbial electrochemical cells)]. An MFC is a device which directly converts, through microbial action, the chemical energy stored in a substrate, including wastes, into electrical energy. These rely on EAB (electroactive bacteria) to transfer electrons through a series of electron-carrier proteins, through the anode, via an external load, through a fuel cell cathode to a terminal electron acceptor, usually oxygen. This process can be exploited in MFCs to generate a considerable amount of power from organic waste [13,14]. The energy value of the fuel, or waste, is harvested in the circuit as electrical power, with complete oxidation of complex organic substrates theoretically producing carbon dioxide and water, thus cleaning the wastewater, as an additional benefit.

In an MEC, the electrons released at the anode from the microbially catalysed oxidation of (waste) substrates are exploited at the cathode where, in the presence of a catalyst (i.e. platinum), a high-value-added product may be generated (e.g. H2, methane or alcohols). The potential at the anode, coupled to a small external energy input needed to drive the otherwise energetically unfavourable cathodic reaction, offsets energy that would otherwise need to be added to drive the process,. However, MXC-based industrial processes have yet to be adopted by the industrial sector. Several fundamental as well as applied challenges, e.g. design and engineering of MFCs for least cost, least resistance, minimized scavenging of electrons, increased current densities and maximized conversion in a sustained manner, remain, and addressing these may provide higher efficiencies and conversion rates in MXCs leading to industrial take-up of these BES technologies.

Bacterial potential for current generation

Bacteria gain energy by transferring electrons from a reduced substrate at a low potential (higher free energy) such as glucose to an electron acceptor with a high potential (lower free energy) such as oxygen. A selection of redox reactions relevant to bacterial electron transfer is given in Table 1 (based on data from [15,16]). If bacteria derive reducing equivalents from glucose in the form of NADH, and subsequently shuttle electrons from NADH to oxygen, the formal potential difference for an MFC is ~1.2 V [ΔE0′=(+0.840 V)−(−0.32 V)]. MFC power output depends on the product of cell voltage and current flowing through the external circuit, usually a fixed resistance load [17]. A maximum OCV (open circuit voltage) of 0.8 V can be observed when there is no current flowing through the external circuit in an MFC [15]. In a closed-circuit MFC, the observed cell voltage decreases significantly as a result of overpotentials. Three kinds of overpotentials can be defined in electrolysis: activation overpotentials, ohmic losses and concentration polarization [18]. Thus overpotential losses mainly depend on the overall fuel cell resistance and the current density flowing through the fuel cell, electrochemical properties of the electrode, the kinetics of electron transfer at and mass transport to the electrodes, and the operational temperature.

Table 1
Common redox reactions, and their formal reduction potentials (compared with the SHE at pH 7 and 25°C)

Data taken from [15,16].

Redox reaction E0′ (mV) 
2H++2e→H2 −420 
Ferredoxin (Fe3+)+e→Ferredoxin (Fe2+−420 
CrO42−+3e+5H+→Cr(OH)3+H2−321 
NAD+H++2e→NADH −320 
S+2H++2e→H2−274 
SO42−+10H++8e→H2S+4H2−220 
Pyruvate2−+2H++2e→lactate2− −185 
FAD+2H++2e→FADH2 −180 
Fumarate2−+2H++2e→succinate2− +31 
Cytochrome b (Fe3+)+e→cytochrome b (Fe2++75 
Ubiquinone+2H++2e→ubiquinone-H2 +100 
U6++2e→U4+ +246 
Cytochrome c (Fe3+)+e→cytochrome c (Fe2++254 
[Fe(CN)6]3−+e→[Fe(CN)6]4− +360 
NO3+2H++2e→NO2+H2+421 
NO2+8H++6e→NH4++2H2+440 
Fe3++e→Fe2+ +771 
Ag++e→Ag(O) +800 
O2+4H++4e→2H2+840 
MnO4+3e+4H+→MnO2+2H2+1138 
Redox reaction E0′ (mV) 
2H++2e→H2 −420 
Ferredoxin (Fe3+)+e→Ferredoxin (Fe2+−420 
CrO42−+3e+5H+→Cr(OH)3+H2−321 
NAD+H++2e→NADH −320 
S+2H++2e→H2−274 
SO42−+10H++8e→H2S+4H2−220 
Pyruvate2−+2H++2e→lactate2− −185 
FAD+2H++2e→FADH2 −180 
Fumarate2−+2H++2e→succinate2− +31 
Cytochrome b (Fe3+)+e→cytochrome b (Fe2++75 
Ubiquinone+2H++2e→ubiquinone-H2 +100 
U6++2e→U4+ +246 
Cytochrome c (Fe3+)+e→cytochrome c (Fe2++254 
[Fe(CN)6]3−+e→[Fe(CN)6]4− +360 
NO3+2H++2e→NO2+H2+421 
NO2+8H++6e→NH4++2H2+440 
Fe3++e→Fe2+ +771 
Ag++e→Ag(O) +800 
O2+4H++4e→2H2+840 
MnO4+3e+4H+→MnO2+2H2+1138 

Researchers have proposed three distinct EET mechanisms to account for electron transfer to solid electrodes, depicted in Figure 1. The first EET mechanism proposes the presence of a soluble electron shuttle, a mediator compound, that is produced by bacteria that diffusively (by physical diffusion or electron-hopping self-exchange) carries electrons to the electrodes. These shuttles can diffuse in and out of the bacterial cell trapping electrons, transporting them to reduce the terminal electron acceptor. Bacteria are known to produce a range of electron-shuttle compounds, such as melanin, phenazines, flavins and quinones [20,21]. A second mechanism for EET is based on direct electron transfer of electrons from bacteria to electron acceptor via OM proteins, such as cytochromes, that can approach the electron acceptor to within a close enough distance to effect electron transfer [22]. A third mechanism proposed is the formation of a biofilm matrix, conductive for electron transfers from the bacteria to the electrode as electron acceptor. An example is the proposal that cellular pili act as conductive nanowires [9,23,24] and/or that electron-hopping self-exchange can occur between cytochromes on the bacteria or in the ECM [4,5] if the reduced and oxidized states can approach each other to within a close enough distance (represented by δ in Figure 1).

Schematic diagram of proposed electron-transfer mechanisms

Figure 1
Schematic diagram of proposed electron-transfer mechanisms

The mechanisms are, from the top, an electron mediator, direct electron transfer and conductive ECM (based on conduction through nanowire pili and/or a self-exchange mechanism; see the text for details). Adapted from Biofuels, July 2010, Vol. 1, No. 4, Pages 589–604, with permission of Future Science Ltd.

Figure 1
Schematic diagram of proposed electron-transfer mechanisms

The mechanisms are, from the top, an electron mediator, direct electron transfer and conductive ECM (based on conduction through nanowire pili and/or a self-exchange mechanism; see the text for details). Adapted from Biofuels, July 2010, Vol. 1, No. 4, Pages 589–604, with permission of Future Science Ltd.

Microbial ecology of EET

Known EAB include members of diverse phyla such as Proteobacteria (including the classes Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria and Deltaproteobacteria), Firmicutes and Acidobacteria [10]. Mostly they are Gram-negative, anaerobic and use Fe(III) as an electron acceptor. Substrate-utilization capabilities of these bacteria are mostly limited to acetate, but some members can utilize a wide range of substrates such as propionate, butyrate, lactate and glucose [13,25,26].

Bacterial attachment to the anode electrode surface is essential for efficient electron transfer in MXCs. Under anaerobic conditions, bacterial cultures reduce a terminal electron acceptor (e.g. iron-respiring bacteria reduce Fe3+ to Fe2+). In a MFC, the anode acts as terminal electron acceptor, and its potential is determined by the potential of the microbially produced electron donor to the electrode (mediator or cytochrome) and the rate of respiration [27]. Therefore the anode potential is related to the relative concentration of reduced and oxidized state of the natural electron acceptor, in a conventional anaerobic respiration process. Bacteria respire only when the anode accepts the electron. Hence, in a three-electrode electrochemical cell, working electrodes can be held at certain applied potentials compared with a reference electrode to mimic the reduction potential of the natural electron acceptor, inducing electron transfer to, and biofilm growth at, the working electrode (acting as an anode).

Figure 2 shows two electrochemical cell set-ups that can be, and have been, used to induce growth of bacterial biofilms by the application of a potential to a working electrode (anode) compared with a reference electrode, with current flowing to a cathode in either the same chamber (Figure 2a) or a separate chamber (Figure 2b), using an proton-exchange membrane, to the working and reference electrodes using a potentiostat. Catalytic current generated by bacterial oxidation of substrate, transferring electrons to the anode, is monitored using chronoamperometry and cyclic voltammetry. This approach lends itself well to high-throughput comparisons as a range of working electrodes can be held at applied potentials in separate electrochemical cells (compared with separate reference and cathode electrodes) or in the same electrochemical cell (compared with a common reference and cathode electrode) using a multichannel device.

Electrochemical cell set-up

Figure 2
Electrochemical cell set-up

The electrochemical cell mimics the anode MFC. (a) Single-chambered cell. (b) Dual-chambered cell.

Figure 2
Electrochemical cell set-up

The electrochemical cell mimics the anode MFC. (a) Single-chambered cell. (b) Dual-chambered cell.

Researchers have used various applied potentials to investigate the EET mechanism of EAB within biofilms of both single and mixed cultures induced to grow on electrodes. In order for the reaction to be thermodynamically favourable, the anode should be held at a potential more positive than the oxidation potential of the substrate, usually acetate (−0.48 V compared with the Ag/AgCl electrode), thermodynamically favouring electron transfer while oxidizing the acetate.

For example, Busalmen et al. [28] showed that different electrochemical responses are observed for Geobacter sulfurreducens films grown under applied potentials of 0.1 V compared with those grown under 0.6 V (compared with the Ag/AgCl electrode in KCl), suggesting two different respiratory processes: one at low anode potential, and the other at higher anode potential [28,29] in dual-chamber electrochemical cells. This bacterium is used as a model for EAB, as it has been shown to perform well in biofilms on electrodes for MFCs, providing among the highest current densities for acetate oxidation in such systems [30]. In the genome of G. sulfurreducens, there are 111 different cytochromes coded, and more than 30 are located in the outer sphere of the cell [28]. ATR-SEIRAS (attenuated total reflection–surface enhanced IR absorption spectroscopy) revealed that the c-type cytochromes present in the outermost location are involved in the electron-transfer process [28,29], and it has been proposed that the bacterial electron-transfer pathway is triggered based on the potential of the electron acceptor [29].

Theoretically, bacteria gain more energy by reducing terminal acceptors at a more positive potential. However, there is no agreed optimal set anode potential using a potentiostat for inducing bacterial growth at the anode. For example, Dumas et al. [31,32] polarized stainless steel and graphite electrodes at different potentials in single-chamber electrochemical cells to induce growth of G. sulfurreducens biofilms. No current was obtained during chronoamperometry at potential values lower than 0.00 V compared with the Ag/AgCl electrode, whereas, at an applied potential of +0.2 V compared with the Ag/AgCl electrode, they observed maximum current densities of 2.4 A·m−2 using stainless steel and 8 A·m−2 using graphite electrodes [31,32]. Marsili et al. [33] reported that an applied potential of 0.16 V compared with the SHE (standard hydrogen electrode) resulted in a much slower growth of biofilms of G. sulfurreducens on carbon disc electrodes placed in single-chamber electrochemical cells, compared with those induced to grow at +0.24 V compared with SHE applied potentials, with distinct differences in the voltammetric signals for single-turnover electrochemistry between the two biofilms formed. There thus remains some uncertainty about the optimum set anode potential for production of biofilms of optimal thickness, or acetate oxidation current, as reported in a recent review [34] and in a recent study [35].

Apart from studies using pure culture, a range of mixed cultures have been inoculated into electrochemical cells and subjected to different applied potentials to investigate biofilm growth and response. Different optimal performances and inconsistent results in selection of applied potentials are reported for such studies, and we provide a selection of these in Table 2. For example, Finkelstein et al. [36] used different anode potentials (−0.058–0.618 V compared with the Ag/AgCl electrode) in a benthic MFC with the more positive applied potential resulting in both higher maximum and more rapid development of acetate oxidation currents. Wang et al. [37] observed more rapid development of acetate oxidation currents for anodes in dual-chambered MFCs polarized at a constant potential (+0.2 V compared with the Ag/AgCl electrode) compared with anodes connected to the cathode across a 1 kΩ resistance load. Other studies using mixed cultures have, however, reported improved biofilm performance when induced to grow at lower applied potentials. For example, Alterman et al. [38] obtained maximum MFC power in a dual-chambered cell for biofilms induced to grow on graphite granular-based anodes using a constant applied potential of −0.2 V compared with the Ag/AgCl electrode, in contrast with those grown using a higher applied potential, with, however, a more active (per biomass unit) biofilm produced at even lower applied potentials (−0.2 V compared with the Ag/AgCl electrode). A combination of microbial ecology and electrochemistry reported previously [27] indicated that biofilms of greater microbial diversity are obtained using higher applied anode potentials, in dual-chambered electrochemical cells, but that higher currents for acetate oxidation were observed for the anodes induced to grow at the lowest (−0.42 V compared with the Ag/AgCl electrode) applied potential studied, with such biofilms dominated by the presence of Geobacter spp.

Table 2
Applied potential studies comparing set anode potentials using a mixed microbial community as inoculum

Potentials are converted into the AgCl scale. N/A, either not available or insufficient information to draw a conclusion. SCE, saturated calomel electrode. * and A. Kumar, A. Siggins, K. Katuri, T. Mahony, V. O'Flaherty, P. Lens, and D. Leech, unpublished work.

Configuration type Applied potentials (V compared with the Ag/AgCl electrode) Working electrode Reported reference electrode Inoculum Start-up Current Reference(s) 
H-cell −0.4, 0, −0.2 Graphite granule Ag/AgCl MFC suspension Similar start-up at all voltages Maximum current at −0.2 V [38
H-cell −0.42, −0.36, −0.25, +0.1 Graphite rods (multiple) Ag/AgCl (0.27 V compared with SHE) Domestic wastewater Faster start-up at 0.42 and −0.36 V 0.42 and −0.36 V showed higher current than others [27
H-cell +0.2, floating potential Graphite plate Ag/AgCl (0.197 V compared with SHE) Domestic wastewater Faster start-up using poised compared with non-poised anode potentials N/A [37
H-cell −0.3,−0.2, +0.2 Graphite rod Ag/AgCl Anaerobic sludge Faster start-up at −0.2 and −0.3 V −0.2 and −0.3 V showed higher current than others [39]* 
S-cell +0.26, +0.46, +0.66 Dimensionally stable anodes (DSA) SCE Garden compost Faster start-up at +0.26 V +0.26 V showed maximum current [40
S-cell −0.058, +0.103, +0.618 Graphite rod Ag/AgCl Marine sediment Faster start-up at +0.618V +0.618 V produced higher current [36
S-cell −0.3, −0.2, +0.2 Graphite rod Ag/AgCl Anaerobic sludge Faster start-up at+0.2 V Maximum current at+0.2 V [39]* 
Configuration type Applied potentials (V compared with the Ag/AgCl electrode) Working electrode Reported reference electrode Inoculum Start-up Current Reference(s) 
H-cell −0.4, 0, −0.2 Graphite granule Ag/AgCl MFC suspension Similar start-up at all voltages Maximum current at −0.2 V [38
H-cell −0.42, −0.36, −0.25, +0.1 Graphite rods (multiple) Ag/AgCl (0.27 V compared with SHE) Domestic wastewater Faster start-up at 0.42 and −0.36 V 0.42 and −0.36 V showed higher current than others [27
H-cell +0.2, floating potential Graphite plate Ag/AgCl (0.197 V compared with SHE) Domestic wastewater Faster start-up using poised compared with non-poised anode potentials N/A [37
H-cell −0.3,−0.2, +0.2 Graphite rod Ag/AgCl Anaerobic sludge Faster start-up at −0.2 and −0.3 V −0.2 and −0.3 V showed higher current than others [39]* 
S-cell +0.26, +0.46, +0.66 Dimensionally stable anodes (DSA) SCE Garden compost Faster start-up at +0.26 V +0.26 V showed maximum current [40
S-cell −0.058, +0.103, +0.618 Graphite rod Ag/AgCl Marine sediment Faster start-up at +0.618V +0.618 V produced higher current [36
S-cell −0.3, −0.2, +0.2 Graphite rod Ag/AgCl Anaerobic sludge Faster start-up at+0.2 V Maximum current at+0.2 V [39]* 

We [39] observed differences in current production for acetate oxidation at graphite rod anodes at biofilms of both single (G. sulfurreducens) and mixed cultures as a function of applied potential, depending on the electrochemical cell configurations (single- and dual-chambered shown in Figure 2) used. Increased anodic currents for bioelectrocatalytic oxidation of acetate were obtained when the electrodes were incubated for longer periods with continuous electron donor feeding. In the single-chambered bioelectrochemical cells, the electrochemical cell polarized at the most positive (most oxidizing) potentials produced the highest current densities for both single- and mixed-culture inocula. However, when using the dual-chambered bioelectrochemical cells (H-cell), the anodes polarized at the more negative potentials showed higher current densities compared with those polarized at more positive potentials.

A better understanding of the physiology and ecology of EAB might be helpful for further bioelectrochemical engineering to achieve high current density, high power and fast start-up in MXCs. Achieving these traits may require setting the anode potential, instead of allowing current to flow through a resistance load, to further understand electron flow through electroactive biofilms. There is no agreed optimal anode potential using a potentiostat to produce either best bacterial growth or performance in terms of current or power density at the anode for MXC applications. Bacteria gain more energy by reducing terminal acceptors at a more positive potential when the bacteria have metabolic pathways capable of capturing the energy available. No one set potential may thus always yield the best results [34], suggesting that the outcome of a set potential experiment is dependent on culture conditions, cell configuration, electrode materials and inocula. Bioelectrochemical investigations of both pure and mixed cultures, over a wide range of potentials, are needed to better understand how to set and evaluate optimal cell configurations and anode potentials for improving MFC performance [34]. Electrochemical tests, community analyses and further study of the response of both pure and mixed cultures at applied potentials and comparison with growth under different external resistance loads (fixed and variable) will improve our understanding of the behaviour of microbial communities in various redox environments.

Electron Transfer at the Microbe–Mineral Interface: A Biochemical Society Focused Meeting held at University of East Anglia, Norwich, U.K., 2–4 April 2012. Organized and Edited by Jim Fredrickson (Pacific Northwest National Laboratory, U.S.A.), David Richardson (University of East Anglia, U.K.) and John Zachara (Pacific Northwest National Laboratory, U.S.A.).

Abbreviations

     
  • BES

    bioelectrochemical system

  •  
  • EAB

    electroactive bacteria

  •  
  • ECM

    extracellular matrix

  •  
  • EET

    extracellular electron transfer

  •  
  • MEC

    microbial electrolysis cell

  •  
  • MFC

    microbial fuel cell

  •  
  • MXC

    microbial electrochemical cell

  •  
  • OM

    outer membrane

  •  
  • SHE

    standard hydrogen electrode

Funding

We acknowledge funding from the European Union Framework Programme 7 People Programme, a Marie Curie Intra European Fellowship (MC-IEF) for Career Development [grant number A/6342-PIEF-GA-2009-237181] and a Science Foundation Ireland Charles Parsons Energy Research Award.

References

References
1
Lovley
D.R.
Extracellular electron transfer: wires, capacitors, iron lungs, and more
Geobiology
2008
, vol. 
6
 (pg. 
225
-
231
)
2
Rosenbaum
M.
Aulenta
F.
Villano
M.
Angenent
L.T.
Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved? Biores
Technol.
2011
, vol. 
102
 (pg. 
324
-
333
)
3
Nealson
K.H.
Finkel
S.E.
Electron flow and biofilms
MRS Bull.
2011
, vol. 
36
 (pg. 
380
-
3082
)
4
Strycharz-Glaven
S.M.
Snider
R.M.
Guiseppi-Elie
A.
Tender
L.M.
On the electrical conductivity of microbial nanowires and biofilms
Energy Environ. Sci.
2011
, vol. 
4
 (pg. 
4366
-
4379
)
5
Strycharz-Glaven
S.M.
Tender
L.M.
Reply to the ‘Comment on “On electrical conductivity of microbial nanowires and biofilms”‘ by N.S. Malvankar, M.T. Tuominen and D.R. Lovley, Energy Environ. Sci., 2012, 5, DOI: 10.1039/c2ee02613a
Energy Environ. Sci.
2012
, vol. 
5
 (pg. 
6250
-
6255
)
6
Nealson
K.H.
Sediment bacteria: who's there, what are they doing, and what's new?
Annu. Rev. Earth Planet. Sci.
1997
, vol. 
25
 (pg. 
403
-
434
)
7
Gralnick
J.A.
Newman
D.
Extracellular respiration
Mol. Microbiol.
2007
, vol. 
65
 
1
(pg. 
1
-
11
)
8
Nielsen
L.P.
Petersen
N.R.
Fossing
H.
Christensen
P.B.
Sayama
M.
Electric currents couple spatially separated biogeochemical processes in marine sediment
Nature
2010
, vol. 
463
 (pg. 
1071
-
1074
)
9
Potter
M.C.
Electrical effects accompanying the decomposition of organic compounds
Proc. R. Soc. London Ser. B
1911
, vol. 
84
 (pg. 
260
-
276
)
10
Kim
H.J.
Hyun
M.S.
Chang
I.S.
Kim
B.H.
A microbial fuel cell type lactate biosensor using a metal-reducing bacterium, Shewanella putrefaciens
J. Microbiol. Biotechnol.
1999
, vol. 
9
 (pg. 
365
-
367
)
11
Reguera
G.
McCarthy
K.D.
Mehta
T.
Nicoll
J.S.
Tuominen
M.T.
Lovley
D.R.
Extracellular electron transfer via microbial nanowires
Nature
2005
, vol. 
435
 (pg. 
1098
-
1101
)
12
Logan
B.E.
Exoelectrogenic bacteria that power microbial fuel cells
Nat. Rev. Microbiol.
2009
, vol. 
7
 (pg. 
375
-
381
)
13
Debabov
V.
Electricity from microorganisms
Microbiology
2008
, vol. 
77
 (pg. 
123
-
131
)
14
Rabaey
K.
Verstraete
W.
Microbial fuel cells: novel biotechnology for energy generation
Trends Biotechnol.
2005
, vol. 
23
 (pg. 
291
-
298
)
15
Madigan
M.T.
Martinko
J.M.
Parker
J.
Brock Biology of Microorganisms
2000
9th edn
Upper Saddle River
Prentice Hall College Division
16
Clauwaert
P.
Rabaey
K.
Angenent
L.
Schröder
U.
Keller
J.
Bioelectrical reductions in reactor systems
Bioelectrochemical Systems: from Extracellular Transfer to Biotechnological Applications
2012
London
IWA
(pg. 
285
-
304
)
17
Niessen
J.
Schroder
U.
Scholz
F.
Exploiting complex carbohydrates for microbial electricity generation-a bacterial fuel cell operating on starch
Electrochem. Commun.
2004
, vol. 
6
 (pg. 
955
-
958
)
18
Larminie
J.
Dicks
A.
Fuel Cell Systems Explained
2000
Chichester
John Wiley & Sons
19
Reference deleted
20
Hernandez
M.E.
Kappler
A.
Newman
D.K.
Phenazines and other redox-active antibiotics promote microbial mineral reduction
Appl. Environ. Microbiol.
2004
, vol. 
70
 (pg. 
921
-
928
)
21
Canstein
H.
Ogawa
J.
Shimizu
S.
Lloyd
J.R.
Secretion of flavins by Shewanella species and their role in extracellular electron transfer
Appl. Environ. Microbiol.
2008
, vol. 
74
 (pg. 
615
-
623
)
22
Beliaev
A.S.
Klingeman
D.M.
Klappenbach
J.A.
Wu
L.
Romine
M.F.
Tiedje
J.M.
Nealson
K.H.
Fredrickson
J.K.
Zhou
J.
Global transcriptome analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors
J. Bacteriol.
2005
, vol. 
187
 (pg. 
7138
-
7145
)
23
Malvankar
N.S.
Vargas
M.
Nevin
K.P.
Franks
A.E.
Leang
C.
Kim
B.C.
Inoue
K.
Mester
T.
Covalla
S.F.
Johnson
J.P.
, et al. 
Tunable metallic-like conductivity in microbial nanowire networks
Nat. Nanotechnol.
2011
, vol. 
6
 (pg. 
573
-
57
)
24
Malvankar
N.S.
Tuominena
M.T.
Lovley
D.R.
Comment on “On electrical conductivity of microbial nanowires and biofilms” by S.M. Strycharz-Glaven, R.M. Snider, A. Guiseppi-Elie and L.M. Tender, Energy Environ. Sci., 2011, 4, 4366
Energy Environ. Sci.
2012
, vol. 
5
 (pg. 
6247
-
6249
)
25
Lovely
D.R.
Dissimilatory metal reduction
Annu. Rev. Microbiol.
1993
, vol. 
47
 (pg. 
263
-
290
)
26
Holmes
D.E.
Bond
D.R.
Lovley
D.R.
Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes
Appl. Environ. Microbiol.
2004
, vol. 
70
 (pg. 
1234
-
1237
)
27
Torres
C.I.
Kato Marcus
A.
Rittmann
B.E.
Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria
Biotechnol. Bioeng.
2008
, vol. 
100
 (pg. 
872
-
881
)
28
Busalmen
J.P.
Esteve-Nuñez
A.
Berná
A.
Feliu
J.M.
ATR-SEIRAS characterization of surface redox processes in G. sulfurreducens
Bioelectrochemistry
2010
, vol. 
78
 (pg. 
25
-
29
)
29
Busalmen
J.P.
Esteve-Nuñez
A.
Feliu
J.M.
Whole cell electrochemistry of electricity-producing microorganisms evidence an adaptation for optimal exocellular electron transport
Environ. Sci. Technol.
2008
, vol. 
42
 (pg. 
2445
-
2450
)
30
Katuri
K.
Ferrer
M.L.
Gutiérrez
M.C.
Jiménez
R.
del Monte
F.
Leech
D.
Three-dimensional microchanelled electrodes in flow-through configuration for bioanode formation and current generation
Energy Environ. Sci.
2011
, vol. 
4
 (pg. 
4201
-
4210
)
31
Dumas
C.
Basseguy
R.
Bergel
A.
Electrochemical activity of Geobacter sulfurreducens biofilms on stainless steel anodes
Electrochim. Acta
2008
, vol. 
53
 (pg. 
5235
-
5241
)
32
Dumas
C.
Basseguy
R.
Bergel
A.
DSA to grow electrochemically active biofilms of Geobacter sulfurreducens
Electrochim. Acta
2008
, vol. 
53
 (pg. 
3200
-
3209
)
33
Marsili
E.
Baron
D.B.
Shikhare
I.D.
Coursolle
D.
Gralnick
J.A.
Bond
D.R.
Shewanella secretes flavins that mediate extracellular electron transfer
Proc. Natl. Acad. Sci. U.S.A.
2008
, vol. 
105
 (pg. 
3968
-
3973
)
34
Wagner
R.C.
Call
D.F.
Logan
B.E.
Optimal set anode potentials vary in bioelectrochemical systems
Environ. Sci. Technol.
2010
, vol. 
44
 (pg. 
6036
-
6041
)
35
Wang
X.
Feng
Y.
Liu
J.
Lee
H.
Ren
N.
Performance of a batch two-chambered microbial fuel cell operated at different anode potentials
J. Chem. Technol. Biotechnol.
2011
, vol. 
8
 (pg. 
590
-
594
)
36
Finkelstein
D.A.
Tender
L.M.
Zeikus
J.G.
Effect of electrode potential on electrode-reducing microbiota
Environ. Sci. Technol.
2006
, vol. 
40
 (pg. 
6990
-
6995
)
37
Wang
X.
Feng
Y.J.
Ren
N.Q.
Wang
H.M.
Lee
H.
Li
N.
Zhao
Q.L.
Accelerated start-up of two-chambered microbial fuel cells: effect of anodic positive poised potential
Electrochim. Acta
2009
, vol. 
54
 (pg. 
1109
-
1114
)
38
Alterman
P.
Freguia
S.
Keller
J.
Verstraete
W.
Rabaey
K.
The anode potential regulates bacterial activity in microbial fuel cells
Appl. Microbiol. Biotechnol.
2008
, vol. 
78
 (pg. 
409
-
418
)
39
Kumar
A.
Siggins
A.
Katuri
K.
Flaherty
V.O.
Lens
P.
Leech
D.
Selective response of anode-respiring bacteria based on constant anode potential in single and dual chambered electrochemical cells
Microbial Resource Management in Biotechnology: Concepts and Applications Conference, Ghent, Belgium, 30 June–1 July 2011
2011
40
Parot
S.
Delia
M.L.
Bergel
A.
Forming electrochemically active biofilms from garden compost under chronoamperometry
Bioresour. Technol.
2008
, vol. 
99
 (pg. 
4809
-
4816
)