Microbial Energizers: FuelCells That Keep on GoingMicrobes that produce electricity by oxidizing organic compounds inbiomass may someday power useful electronic devices

Derek R. Lovley

Has this happened to you? You havea layover between flights, wouldlike to use your computer and cellphone, but both sets of batteriesare drained and the nearby electri-

cal outlets are being used. What if you couldinstead recharge your electronic devices with alittle sugar from the nearby coffee stand? Withhelp from electricity-producing microorgan-isms, known as electricigens, some day youmight have new options for ignoring the current“grid” by generating electricity in an alternative,environmentally friendly manner.

Electricigens are recently discovered microor-

ganisms with the ability to oxidize organic com-pounds to carbon dioxide while transferringelectrons to electrodes with extraordinarily highefficiencies. Electricigens make it possible toconvert renewable biomass and organic wastesdirectly into electricity without combusting thefuel, which wastes substantial amounts of en-ergy as heat. Efforts to eliminate the inefficien-cies of combustion are behind the recent interestin hydrogen fuel cells, which oxidize hydrogenand reduce oxygen to water while producingelectricity in a controlled chemical reaction.

With electricigens, however, it becomes pos-sible to make microbial fuel cells, which offer

potential advantages over hydrogen fuelcells. For example, hydrogen fuel cells re-quire a very pure source of a highly explo-sive gas that is difficult to store and distrib-ute. Furthermore, hydrogen is derivedmainly from fossil fuel rather than renew-able sources. In contrast, the energy sourcesfor microbial fuel cells are renewable organ-ics, including some that are dirt cheap.

Geobacteraceae Producing

Electricity in Mud

Several years ago, Leonard Tender of theNaval Research Laboratories in Washing-ton, D.C., and Clare Reimers of OregonState University in Corvallis developed sys-tems in which electricigens produce electric-ity from mud! When a slab of graphite (theanode) is buried in anaerobic marine sedi-ments and then connected to another pieceof graphite (the cathode) that is suspendedin the overlying aerobic water, electricity

Summary

• Electricigenic microorganisms such asGeobacter and Rhodoferax efficiently oxidizeorganic compounds to carbon dioxide whiledirectly transferring electrons to electrodes.

• Electricigen-based microbial fuel cells mark aparadigm shift because these cells completelyoxidize organic fuels while directly transferringelectrons to electrodes without mediators.

• Although microbial fuel cells are unlikely toproduce enough electricity to contribute to thenational power grid in the short-term, the cellsmay prove feasible in some specific instancessuch as covering the local energy needs for pro-cessing food wastes.

• Optimizing microbial fuel cells will entail devel-oping a better understanding of how electrontransfers occur along the outer surfaces of elec-tricigens; key challenges include increasing an-ode surface areas and increasing electricigenrespiration rates.

Derek R. Lovley isDistinguished Uni-versity Professorand Director of En-vironmental Bio-technology at theUniversity of Mas-sachusetts, Am-herst.

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flows between them (Fig. 1). Although this ar-rangement typically produces meager electricalcurrents, they are adequate for running analyticmonitoring devices similar to those that investi-gators place in remote locations such as theocean bottom.

How do such sediment fuel cells produce elec-tricity? The simple answer is, with microbes.Dawn Holmes, working with Daniel Bond inmy laboratory, scraped the anode surface witha razor blade, extracted DNA from thosescrapings, and determined what species werepresent based on their 16S rRNA genes. Thesurprising result is that such anodes are highlyenriched with microorganisms in the familyGeobacteraceae. When similar pieces of graph-ite are incubated in sediments but not connectedto a cathode in overlying water, there is no suchenrichment.

Which Geobacteraceae prove to be prevalentin such samples depends on the specific environ-ment being tested. For example, if electrodes areplaced in marine sediments, Desulfuromonasspecies predominate, whereas if the electrodesare placed in freshwater sediments, Geobacterspecies predominate. Although Geobacter andDesulfuromonas species have similar physiolo-gies, Desulfuromonas prefer marine salinity,while Geobacter favor freshwater.

A hallmark of Geobacteraceae is their abilityto transfer electrons onto extracellular electronacceptors. For example, Geobacter and Desul-furomonas species support growth by couplingthe oxidation of organic compounds to the re-duction of Fe(III) or Mn(IV) oxides. Further-more, these microorganisms can transfer elec-trons to other metals and to the quinonemoieties of humic substances, which are so large

F I G U R E 1

Sediment fuel cell. (A) Prior to deployment in salt marsh sediments on Nantucket Island, Mass. (B) Diagram of sediment fuel cell reactions.(C) Deployed sediment fuel cells. (Photos courtesy of Kelly Nevin, University of Massachusetts-Amherst.)

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that they must be reduced outside bac-terial cells. Reducing Fe(III) oxides is animportant means for degrading organicmatter in aquatic sediments, submergedsoils, and subsurface environments. Mo-lecular analyses of such environments re-veal that, in general, Geobacteraceae arethe predominant Fe(III)-reducing micro-organisms in zones in which Fe(III) re-duction is important.

Holmes and Bond found thatGeobacteraceae can also use electrodesas extracellular electron acceptors.Both Desulfuromonas and Geobacterspecies can grow by oxidizing organiccompounds to carbon dioxide, withelectrodes serving as the sole electronacceptor. Moreover, more than 95% ofthe electrons derived from oxidizingsuch organic matter can be recovered aselectricity. In sediment fuel cells,Geobacteraceae oxidize organic com-pounds but, instead of transferring elec-trons to Fe(III) or Mn(IV), their naturalelectron acceptors, they transfer elec-trons onto electrodes (Fig. 1). The elec-trons flow through the electrical circuitto the cathode, where they react withoxygen to form water.

Self-Perpetuating, Highly Efficient,

Geobacter-Based Microbial Fuel Cells

The sediment fuel cell can be recreated with purecultures of Geobacter (Fig. 2). The anaerobicanode chamber contains organic fuel and agraphite electrode. The cathode chamber has asimilar electrode and is aerobic. Geobactertransfers electrons released from oxidized or-ganic matter onto the anode. The electrons flowfrom the anode to the cathode. The two cham-bers are separated by a cation-selective mem-brane that permits the protons that are releasedfrom oxidized organic matter to migrate to thecathode side, where they combine with electronsand oxygen to form water.

The cation-selective membrane limits oxygendiffusion to the anode chamber, preventingGeobacter from oxidizing the organic fuels withthe direct reduction of oxygen. By inserting anelectrical circuit within the flow of electrons tooxygen, energy can be harvested that otherwise

would go to the electricigenic microbe via aero-bic respiration. However, the electricigens stillrecover some energy from electron transfer tothe electrode. This energy recovery is very im-portant because the energy that the electricigensconserve allows them to maintain viability andto produce electricity as long as fuel is provided.

Nearly a century ago, M. C. Potter at theUniversity of Durham in England measuredelectrical currents when electrodes were placedin microbial cultures. In this and other studiescarried out throughout much of the 20th cen-tury, microbes generated electricity by produc-ing soluble, reduced compounds that could reactabiotically with electrode surfaces. In initialstudies these were natural reduced end productsof fermentation or anaerobic respiration such ashydrogen, sulfide, alcohols, or ammonia. How-ever, many of these reduced products react onlyslowly with electrodes, and other end products,such as organic acids, do not appreciably reactwith electrodes at all. Adding soluble electronacceptors, known as electron shuttles or media-tors, enhances current production in such sys-

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Volume 1, Number 7, 2006 / Microbe Y 325

tems. These electron shuttles enter cells in theoxidized form, accept electrons from respiratorycomponents within the cell, exit in reduced form,and donate electrons to an electrode, whichrecycles them into the oxidized form. However,there are drawbacks to using such mediators—they add expense to electricity production, andmany of them are toxic to humans and/or unsta-ble. Mediators are especially unsuitable for elec-tricity-generating strategies in open environ-ments. Furthermore, the microbes used in thesesystems typically were fermentative and thusmost of the electrons available in the organicfuel remained in organic products instead ofbeing transferred to the electrodes.

More recently, studies in the laboratory ofByung Hong Kim at the Korea Institute of Sci-ence and Technology demonstrated that fuelcells containing Shewanella species could pro-duce electricity from lactate without the addi-tion of electron shuttles. However, the efficiencyof electron transfer was low in part becauseShewanella species only incompletely oxidizelactate to acetate.

Geobacter-Based Fuel Cells

Mark a Paradigm Shift

Although a few years ago fuel cell ex-perts thought that direct electrochemi-cal contact between microorganisms andelectrodes was virtually impossible, thismechanism appears to be how Geo-bacteraceae carry out electron transferto electrodes. Thus, the use of Geo-bacteraceae in microbially based fuelcells marks a paridigm shift. They com-pletely oxidize organic fuels to carbondioxide while directly transferring elec-trons to electrodes without mediators.There has been no known evolutionarypressure on microorganisms to produceelectricity. Therefore, it is hypothesizedthat Geobacter cells transfer electronsto electrodes via the same mechanismsthat they use when reducing extracellu-lar, insoluble electron acceptors, suchas Fe(III) oxides, that they encounter innatural environments.

Evidence for direct electron transferfrom Geobacteraceae to electrodescomes from a variety of studies. For

instance, Kelly Nevin at UMASS-Amherst dem-onstrated that G. metallireducens has to directlycontact Fe(III) oxides to reduce them. DanielBond found that the cells of closely related G.sulfurreducens that attach to electrode surfaces(Fig. 3), rather than planktonic cells, are respon-sible for producing power in microbial fuel cells.Electrochemically active proteins on the outersurface of G. sulfurreducens could serve as elec-trical contact points between the microbes andelectrode surfaces.

If the electrode is adjusted to a low enoughpotential, it can act as an electron donor forGeobacter species, rather than an electron accep-tor, according to Kelvin Gregory in my lab. Labo-ratory studies have suggested that this processmight be used to provide Geobacter with electronsto remove contaminants, such as uranium, frompolluted water via reductive precipitation.

Electricigens Other than Geobacteraceae

Microorganisms outside the Geobacteraceaefamily can also oxidize organic compounds tocarbon dioxide, with electrodes serving as thesole electron acceptor. For example, SwadesChaudhuri from my lab found that Rhodoferax

F I G U R E 3

Transmission electron micrograph of Geobacter covering graphite anode. (Photo cour-tesy of Daniel Bond, University of Massachusetts-Amherst.)

326 Y Microbe / Volume 1, Number 7, 2006

ferrireducens can completely oxidize sugarswith electron transfer to electrodes.

Sugars are important constituents of manywastes and renewable biomass. AlthoughGeobacter species oxidize a variety of organicacids and aromatic compounds as well as hydro-gen, none appears to oxidize sugars. Therefore,producing electricity from sugars withGeobacter species also requires fermentative mi-croorganisms to convert those sugars to organicacids and hydrogen. Rhodoferax offers the pos-sibility of directly converting these sugars toelectricity with a single organism.

In sediment fuel cells that we tested in fresh-water sediments, we detected 16S rRNA genesequences on the anodes that appear closelyrelated to Geothrix fermentans, although atmuch lower levels than Geobacter sequences. G.ferementans is an acetate-oxidizing Fe(III) re-ducer, and Daniel Bond found that G. fermen-tans can also oxidize acetate with the produc-tion of electricity. The G. fermentans cellsappear to be enmeshed in an extracellular ma-trix on the electrode, in contrast withGeobacter-covered electrodes, which carry lit-tle, if any, extracellular material. We speculatethat Geothrix produces this material to limitlosses of an electron shuttling compound it re-leases and that the high energetic cost of produc-ing a shuttle limits the ability of Geothrix tocompete with Geobacter species on electrodes.

In marine sediments with high concentrationsof sulfide, electrodes may also be colonized bymicroorganisms in the family Desulfobul-baceae, according to my colleague DawnHolmes. Sulfide can react directly with elec-trodes, where it is oxidized to elemental sulfur.Desulfobulbus propionicus, a Fe(III)-reducingrepresentative of the Desulfobulbaceae, can ox-idize elemental sulfur to sulfate with an elec-trode as the electron acceptor. Thus, when sul-fate reducers are actively involved in degradingorganic matter in marine sediments, sulfidemight serve as an electron carrier that can begenerated at a distance from the electrode sur-face—providing electrons for electricity fromboth abiotic and biotic reactions.

It seems likely that many other types of micro-organisms can directly transfer electrons to elec-trodes, and some of them may have propertieswith practical significance. Furthermore, if thecapacity for direct electron transfer to electrodesis a general characteristic of microorganisms

capable of reducing Fe(III), it may be possible toproduce electricity under extreme conditions.Most notably, the capacity for reducing Fe(III) ishighly conserved among hyperthermophilic bac-teria and archaea.

Potential Practical Applications

for Fuel Cells

The primary near-term practical application offuel cells powered by electricigens is likely to besediment fuel cells designed to power electronicmonitoring equipment in remote locations.However, electricigens can extract electricityfrom a wide range of other sources of microbi-ally degradable organic wastes or renewablebiomass. Although oxidizing these organic fuelsyields carbon dioxide, this process returns onlyrecently fixed carbon to the atmosphere andthus is not a net contributor to atmosphericcarbon levels. Furthermore, oxidizing these ma-terials in fuel cells would produce none of thepollutants usually associated with combustion.When wastes are the energy source, potentialenvironmental contaminants are consumedwhile producing electricity.

Kelvin Gregory in my lab showed that micro-bial fuel cells can convert swine wastes to elec-tricity, avoiding the usual waste-handling pro-cess that releases methane and odor-causingorganic acids. In his studies, Geobacteraceaeaccounted for more than 70% of the microbesliving on the surface of anodes that were im-mersed in the swine waste.

Meanwhile, Willy Verstraete at Ghent Uni-versity in Ghent, Belgium, and Bruce Logan atPennsylvania State University in UniversityPark, among others, are designing reactors forefficiently converting high volumes of animalwastes and human sewage into electricity.Which microorganisms are producing electricityin these systems is not well understood, butorganisms other than Geobacteraceae typicallypredominate.

Microbial fuel cells that produce enough elec-tricity from organic wastes are unlikely to sub-stantially contribute to the national power gridin the short term. Not only would such a systembe an engineering marvel but, even if optimized,it would be difficult to compete with othersources of relatively cheap electricity, such asfossil fuels and nuclear fission. Nonetheless, mi-crobial fuel cells may prove practical sooner for

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some relatively high-energy liquid wastes, suchas those from processing food or milk, whereelectricity generation could help to cover treat-ment costs.

Another short-term practical applicationcould be the powering of electronic deviceswithout connecting them to the grid—espe-cially, say, in developing countries where micro-organisms are widely used to convert domesticwaste to methane gas that is used locally forcooking. Converting such wastes to electricityinstead of methane would provide greater versa-tility. Another possibility is to develop aquaticor terrestrial “gastrobots,” robots that consumeorganic matter to power their locomotion andsensing and computational needs.

Meanwhile, Bruce Rittman at Arizona StateUniversity and his collaborators are evaluatingwhether microbial fuel cells can be designed touse astronaut wastes as an electric energy sourceduring space travel. More down to earth, otherengineers are considering whether microbialfuel cells could provide energy for mobile elec-tronic devices or automobiles.

Fuel Cells Need Optimizing before

Applications Become Common

Why are some of these applications notyet in place? For one thing, electricigenswere discovered only recently. For an-other, they produce power slowly, suit-able for low-energy devices such assimple calculators (Fig. 4) or as trickle-charging devices for traditional batter-ies (see www.geobacter.org). In orderfor microbial fuel cells to power a widerassortment of electronic devices, thecells will need to oxidize fuels morerapidly than they now can.

A key design challenge is to increaseanode surface areas because of the di-rect relationship between anode surfacearea and power output. Other electro-chemical considerations include ensur-ing that internal resistances and oxygenreduction rates at the cathode do notrestrict electron flow.

Optimizing microbial fuel cells willalso entail developing a better under-standing of how electricgens transferelectrons from their outer surface onto

anodes. As we learn more about the electricalcontacts between microbes and electrodes, wecan begin to develop materials for electrodesthat better interact with the electron transferproteins of the electricigens. Moreover, wecan perhaps genetically engineer these microbesto produce more or better contacts with elec-trodes.

We are evaluating several outer-membraneproteins that might serve as electrical contactpoints between G. sulfurreducens and fuel-cellelectrodes. One candidate is a highly abundantc-type cytochrome, OmcS, that is displayed onthe outside of the cell. Teena Mehta in my labdemonstrated that OmcS is required for extra-cellular electron transfer onto Fe(III) oxides.Another candidate is pili, according to GemmaReguerra in my lab and Kevin McCarthy andMark Tuominen in the University of Massachu-setts-Amherst Physics Department. They dem-onstrated that G. sulfurreducens pili are electri-cally conductive and function as microbialnanowires (Fig. 5). Genetic studies and the phys-ical location of the pili suggest that they canserve as the final conduit for electron transferbetween the cell and the Fe(III) oxides.

F I G U R E 4

Geobacter fuel cells powering a calculator. (Photo courtesy of Kelly Nevin, University ofMassachusetts-Amherst.)

328 Y Microbe / Volume 1, Number 7, 2006

Another path to increasing the elec-tricity output of microbial fuelcells may be to increase Geobacter’srespiration rate. Mounir Izallalen frommy laboratory and RadhakrishnanMahadevan at Genomatica, Inc., in SanDiego, Calif., used a genome-basedmodel of G. sulfurreducens to formu-late a strategy for increasing its respira-tion rate. They then used genetic engi-neering to produce cells that respiredfaster.

These efforts to understand howGeobacter and other electricigens pro-duce electricity come when marketforces encourage development ofsmaller, more efficient electronic de-vices as well as alternative sources forincreasingly costly fossil fuels. Hence,further study of electricigens not onlywill provide valuable insights into theelegance of extracellular electron trans-fer but could also lead to novel engi-neering concepts that bring practicalbenefits to consumers.

SUGGESTED READING

Bond, D. R., D. E. Holmes, L. M. Tender, and D. R. Lovley. 2002. Electrode-reducing microorganisms harvesting energy frommarine sediments. Science 295:483–485.Chaudhuri, S. K., and D. R. Lovley. 2003. Electricity from direct oxidation of glucose in mediator-less microbial fuel cells.Nature Biotechnol. 21:1229–1232.Gregory, K. B., and D. R. Lovley. 2005. Remediation and recovery of uranium from contaminated subsurface environmentswith electrodes. Environ. Sci. Technol. 39:8943–8947.Logan, B. E. 2005. Simultaneous wastewater treatment and biological electricity generation. Water Sci. Technol. 52:31–37.Lovley, D. R. 2006. Bug juice: harvesting energy with microorganisms. Nature Rev. Microbiol., in press.Rabaey, K., and W. Verstraete. 2005. Microbial fuel cells: novel biotechnology for energy generation. Trends. Biotechnol.6:291–298.Reguera, G., K. D. McCarthy, T. Mehta, J. Nicoll, M. T. Tuominen, and D. R. Lovley. 2005. Extracellular electron transfervia microbial nanowires. Nature 435:1098–1101.Shukla, A. K., P. Suresh, S. Berchmans, and A. Rahjendran. 2004. Biological fuel cells and their applications. Curr. Sci.87:455–468.

F I G U R E 5

Transmission electron micrograph of the abundant electrically conductive pili ofGeobacter sulfurreducens. (Photo courtesy of Gemma Reguera, University of Massa-chusetts-Amherst.)

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