COBIOT-854; NO. OF PAGES 8 Please cite this article in press as: Lovley DR, Nevin KP. A shift in the current: New applications and concepts for microbe-electrode electron exchange, Curr Opin Biotechnol (2011), doi:10.1016/ j.copbio.2011.01.009 Available online at www.sciencedirect.com A shift in the current: New applications and concepts for microbe-electrode electron exchange Derek 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 Introduction Electrodes 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. 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 www.sciencedirect.com Current Opinion in Biotechnology 2011, 22:1–8
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COBIOT-854; NO. OF PAGES 8
Available online at www.sciencedirect.com
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
A shift in the current: New applications and concepts for microbe-electrode electron exchange Lovley and Nevin 3
COBIOT-854; NO. OF PAGES 8
Figure 2
PowerSupply
PCE
PCE PCE
DCE
DCE DCEDCE
DCE
DCE
PCE
DCE
GW flow
Cathode
Anode
O2 CO2
H2O
e-
Current Opinion in Biotechnology
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-
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
1. Lovley DR: Powering microbes with electricity: direct electrontransfer from electrodes to microbes. Environ Microbiol Rep2010 doi: 10.1111/j.1758-2229.2010.00211.x.
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.
5. Tender LM, Gray SM, Groveman E, Lowy DA, Kauffman P,Melhado J, Tyce RC, Flynn D, Petrecca R, Dobarro J: The firstdemonstration of a microbial fuel cell as a viable powersupply: powering a meterological buoy. J Power Sources 2008,179:571-575.
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8. Dewan A, Donovan C, Heo D, Beyenal H: Evaluating theperformance of microbial fuel cells powering electronicdevices. J Power Sources 2010, 195:90-96.
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10.��
Dewan A, Beyenal H, Lewandowski Z: Scaling up microbial fuelcells. Environ Sci Technol 2008, 42:7643-7648.
Demonstration that microbial fuel cells do not scale in a linear manner.
11.��
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.
12. Cusick RD, Kiely PD, Logan BE: A monetary comparison ofenergy recovered from microbial fuel cells and microbialelectrolysis cells fed winery or domestic wastewaters. Int JHydrogen Energy 2010, 35:8855-8861.
Please cite this article in press as: Lovley DR, Nevin KP. A shift in the current: New applications an
Excellent review of this novel bioenergy strategy.
15. Rozendal RA, Leone E, Keller J, Rabaey K: Efficient hydrogenperoxide generation from organic matter in a bioelectricalsystem. Electrochem Commun 2009, 11:1752-1755.
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18. Thrash JC, Coates JD: Review: direct and indirect electricalstimulation of microbial metabolism. Environ Sci Technol 2008,42:3921-3931.
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26.�
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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d concepts for microbe-electrode electron exchange, Curr Opin Biotechnol (2011), doi:10.1016/
A shift in the current: New applications and concepts for microbe-electrode electron exchange Lovley and Nevin 7
COBIOT-854; NO. OF PAGES 8
32. Strycharz SM, Woodward TL, Johnson JP, Nevin KP, Sanford RA,Loeffler FE, Lovley DR: Graphite electrode as a sole electrondonor for reductive dechlorination of tetrachlorethene byGeobacter lovleyi. Appl Environ Microbiol 2008, 74:5943-5947.
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.
34. Aulenta F, Reale P, Canosa A, Rossetti S, Panero S, Majone M:Characterization of an electro-active biocathode capable ofdechlorinating trichloroethene to ethene. Biosens Bioelectron2010, 25:1796-1802.
35. Butler C, Clauwaert P, Green SJ, Verstraete W, Nerenberg R:Bioelectrochemical perchlorate reduction in a microbial fuelcell. Environ Sci Technol 2010, 44:4685-4691.
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39.��
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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.
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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.
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in extracellular electron transfer. Energy Environ Sci 2009,2:506-516.
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51. Lovley DR: Extracellular electron transfer: wires, capacitors,iron lungs, and more. Geobiology 2008, 6:225-231.
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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.
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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.
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59.�
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New model for coupling electron flow through pili and cytochromes forextracellular electron transfer.
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In depth analysis of electron transfer through Geobacter sulfurrreducensanode biofilms identifying the key aspects of this process.
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