Microbial Electrosynthesis: Feeding Microbes Electricity To Convert
Carbon Dioxide and Water to Multicarbon Extracellular Organic
Kelly P. Nevin, Trevor L. Woodard, Ashley E. Franks, Zarath M. Summers, and Derek R. Lovley
Department of Microbiology, University of Massachusetts, Amherst, Massachusetts, USA
ABSTRACT The possibility of providing the acetogenic microorganism Sporomusa ovata with electrons delivered directly to the
cells with a graphite electrode for the reduction of carbon dioxide to organic compounds was investigated. Biofilms of S. ovata
Received 1 April 2010 Accepted 5 May 2010 Published 25 May 2010
Citation Nevin, K. P., T. L. Woodard, A. E. Franks, Z. M. Summers, and D. R. Lovley. 2010. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and
water to multicarbon extracellular organic compounds. mBio 1(2):e00103-10. doi:10.1128/mBio.00103-10.
Editor Rita R. Colwell, University of Maryland
Copyright © 2010 Nevin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported
License, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
Address correspondence to Derek R. Lovley, email@example.com.
capture the electrical energy produced from these sources in co-
valent chemical bonds, producing compounds that can readily be
stored and consumed on demand, preferably within the existing
infrastructure (1). One particularly attractive option is to reduce
carbon dioxide to produce multicarbon organic compounds that
are precursors for desirable organic chemicals or liquid transpor-
tation fuels (2). Basic requirements for a practical system to fix
carbon dioxide in this manner include (i) the ability to use elec-
trons derived from water as an abundant, inexpensive source of
reductant (1, 2); and (ii) inexpensive, durable catalysts (3).
Reaction thermodynamics suggests that it should be readily
feasible to electrochemically reduce carbon dioxide to a diversity
of organic compounds, and this process has been studied for over
ical reduction of carbon dioxide has not proven practical in large
part due to (i) poor long-term stability of the cathodes, (ii) non-
specificity of products produced, (iii) sluggishness of carbon di-
(v) cathode expense (3). Incorporating enzyme catalysts on elec-
trodes may promote more specific product formation from elec-
trochemical reduction of carbon dioxide and lower the energy
required for reduction (3), but experiments on enzymatic reduc-
he intermittent nature of renewable sources of energy, most
notably solar and wind, is leading to a search for strategies to
Acetogenic bacteria can reduce carbon dioxide to acetate and
other multicarbon extracellular products with hydrogen as the
electron donor (6, 7). However, supplying acetogens with hydro-
gen that is produced electrochemically is unlikely to be practical
because it would require expensive catalysts and/or substantial
energy inputs (8). An alternative might be to directly feed aceto-
gens electrons with electrodes. Geobacter and Anaeromyxobacter
species have previously been shown to accept electrons from
the reduction of nitrate to nitrite (9), U(VI) reduction (10), or
electrons at electrode surfaces for carbon dioxide reduction to
methane (13), but this has been difficult to verify because there
electrode potentials required for active methanogenesis (14).
acetogen electrons from an electrode with Sporomusa ovata (15)
(Deutsche Sammlung Mikroorganismen und Zellkulturen
May/June 2010 Volume 1 Issue 2 e00103-10
cathode and anode were comprised of unpolished graphite sticks.
The anode and cathode chambers, each containing 200 ml of me-
dium, were separated with a Nafion cation-exchange membrane.
A potentiostat maintained a potential difference between the an-
delivered to the cathode at ?400 mV (versus standard hydrogen
electrode), a potential well above the ?600 mV necessary to pro-
duce even low levels of hydrogen with unpolished graphite (8).
The lack of hydrogen production was verified by directly measur-
obtained from a standard electrical outlet, but a solar-powered
trol unit built with standard electrical components, could also
support the system.
An inoculum of S. ovata was grown with hydrogen as the elec-
tron donor (H2-CO2 [80:20]) in the DSMZ-recommended
growth medium (DSMZ 311) with betaine, Casitone, and resa-
zurin omitted. The hydrogen-grown cells were introduced into
the cathode chamber in the same medium but with the yeast ex-
tract and the cysteine and sulfide reductants omitted. This
bicarbonate-based medium contained no organic compounds
other than a vitamin mixture, and carbon dioxide was the sole
electron acceptor. The culture was initially bubbled with a
hydrogen-containing gas mixture (N2-CO2-H2[80:13:7]) as an
additional electron donor to accelerate the growth of a biofilm on
the cathode surface. Acetate was measured with high-
performance liquid chromatography (HPLC) (16). Once acetate
reached 10 mM, 50% of the medium was replaced with fresh me-
dium. This process was repeated three times. This periodic re-
moval of planktonic cells promoted biofilm growth on the cath-
consumption of current was observed (within 24 h), the system
tained under N2-CO2was continuously introduced (0.1 ml/min;
gen partial pressures in the headspace remained less than 10 ppm
throughout the study, ca. 2 orders of magnitude below the mini-
mum threshold for acetate production from hydrogen by aceto-
Systems with S. ovata steadily consumed current with the pro-
duction of acetate and small amounts of 2-oxobutyrate (Fig. 1b).
Uninoculated controls did not consume current or produce or-
ganic acids. If the current supply to the S. ovata biofilm was inter-
rupted, acetate and 2-oxobutyrate production stopped.
Although it was not possible to measure carbon dioxide con-
sumption due to the high concentrations of bicarbonate in the
appearing in acetate accounted for a high proportion of the elec-
trons that the cultures consumed (Fig. 1b). In three replicate cul-
? 21% of the electrons transferred at the cathodes. These results
demonstrated that S. ovata could accept electrons from graphite
electrodes with the reduction of carbon dioxide and that most of
the electrons transferred from the electrodes to the cells were di-
verted toward extracellular products, rather than biomass forma-
for periods of more than 3 months without losing their capacity
for current consumption and acetate production.
from confocal scanning laser microscopy of a biofilm that had
been fixing carbon dioxide for 3 months. The cells in biofilms
treated with LIVE/DEAD BacLight viability stain, as previously
and metabolically active (Fig. 2a). The biofilms were relatively
thin, similar to the biofilms previously described for other micro-
organisms growing on cathodes (9, 11, 12). This was further con-
(Fig. 2b), prepared as previously described (19). The cells ap-
FIG 1 (a) H-cell device for supplying cathode biofilms of S. ovata electrons derived from water. The solar-powered option is illustrated. 8 e?, 8 electrons. (b)
electric current. The mean standard errors of the organic acid and current measurements were 2% and 13%, respectively.
Nevin et al.
mbio.asm.orgMay/June 2010 Volume 1 Issue 2 e00103-10
peared to be intimately associated with the graphite surface, as
11, 12). There was no visible turbidity in the cathode chamber,
consistent with previous studies on direct electrode-driven respi-
ration (9–12) and further suggesting that biofilm cells were pri-
marily responsible for current consumption and carbon dioxide
Implications. These results demonstrate that S. ovata is capa-
donor for the reduction of carbon dioxide to acetate. The high
in acetate/electrons consumed as current) are consistent with the
following reaction: 2CO2? 2 H2O ¡ CH3COOH ? 2O2.
This conversion of carbon dioxide and water to an organic
compound and oxygen is the same net reaction as oxygenic pho-
tosynthesis. We propose the term microbial electrosynthesis for
the reduction of carbon dioxide to multicarbon compounds with
bial electrosynthesis differs significantly from photosynthesis in
that carbon and electron flow is directed primarily to the forma-
tion of extracellular products, rather than biomass. Biomass typ-
production. When coupled to a photovoltaic system, microbial
electrosynthesis offers a new photosynthetic technology for the
production of organic products with the added advantage that
photovoltaic technology is orders of magnitude more effective in
capturing solar energy than photosynthesis is (20).
Although acetate has economic value (6), a more important
consideration is that acetate is formed from acetyl coenzyme A
(acetyl-CoA) (6, 7), which is the central intermediate for the ge-
modities as well as potential liquid transportation fuels (21, 22).
The fact that small amounts of 2-oxobutyrate were produced, in
ing, some carbon and electron flow was diverted away from ace-
tanol from acetyl-CoA (23). Attempts to genetically engineer
S. ovata and other acetogens to produce products other than ace-
tate via microbial electrosynthesis are under way.
This research was supported by the Office of Science (BER), U.S Depart-
ment of Energy, Cooperative Agreement DE-FC02-02ER63446.
discussions that led to the development of this project.
1. Lewis, N. S., and D. G. Nocera. 2006. Powering the planet: chemical
challenges in solar energy utilization. Proc. Natl. Acad. Sci. U. S. A. 103:
2. Centi, G., and S. Perathoner. 2009. Opportunities and prospects in the
chemical recycling of carbon dioxide to fuels. Catal. Today 148:191–205.
3. Cole, E. B., and A. B. Bocarsly. 2010. Photochemical, electrochemical,
Co., Weinheim, Germany.
4. Gattrell, M., N. Gupta, and A. Co. 2006. A review of the aqueous
electrochemical reduction of CO2to hydrocarbons at copper. J. Electro-
anal. Chem. 594:1–19.
5. Olomon, C., and H. Li. 2008. Electrochemical processing of carbon
dioxide. ChemSusChem 1:385–391.
6. Drake, H. L., A. S. Gössner, and S. L. Daniel. 2008. Old acetogens, new
light. Ann. N. Y. Acad. Sci. 1125:100–128.
7. Muller, V. 2003. Energy conservation in acetogenic bacteria. Appl. Envi-
ron. Microbiol. 69:6345–6353.
8. Aulenta, F., P. Reale, A. Catervi, S. Panero, and M. Majone. 2008.
Kinetics of trichlorethene dechlorination and methane formation by a
mixed anaerobic culture in a bio-electrochemical system. Electrochim.
9. Gregory, K. B., D. R. Bond, and D. R. Lovley. 2004. Graphite electrodes
as electron donors for anaerobic respiration. Environ. Microbiol.
10. Gregory, K. B., and D. R. Lovley. 2005. Remediation and recovery of
uranium from contaminated subsurface environments with electrodes.
Environ. Sci. Technol. 39:8943–8947.
11. Strycharz, S. M., S. M. Gannon, A. R. Boles, K. P. Nevin, A. E. Franks,
and D. R. Lovley. 2010. Anaeromyxobacter dehalogenans interacts with a
Environ. Microbiol. Rep. 2:289–294.
12. Strycharz, S. M., T. L. Woodward, J. P. Johnson, K. P. Nevin, R. A.
Sanford, F. E. Loeffler, and D. R. Lovley. 2008. Graphite electrode as a
sole electron donor for reductive dechlorination of tetrachlorethene by
Geobacter lovleyi. Appl. Environ. Microbiol. 74:5943–5947.
13. Cheng, S., D. Xing, D. F. Call, and B. E. Logan. 2009. Direct biological
conversion of electrical current into methane by electromethanogenesis.
Environ. Sci. Technol. 43:3953–3958.
14. Villano, M., F. Aulenta, C. Ciucci, T. Ferri, A. Giuliano, and M. Majone.
2010. Bioelectrochemical reduction of CO2to CH4via direct and indirect
extracellular electron transfer by a hydrogenophilic methanogenic cul-
ture. Bioresource Technol. 101:3085–3090.
15. Moller, B., R. Obmer, B. H. Howard, G. Gottschalk, and H. Hippe.
ing Sporomusa sphaeroides spec. nov. and Sporomusa ovata spec. nov.
Arch. Microbiol. 139:388–396.
16. Nevin, K. P., H. Richter, S. F. Covalla, J. P. Johnson, T. L. Woodard, H. Jia,
M. Zhang, and D. R. Lovley. 2008. Power output and columbic efficiencies
FIG 2 Cathode biofilms of S. ovata. (a) Confocal scanning laser microscopic images (top down and side views) of cathode surface. Cells were stained with
LIVE/DEAD BacLight viability stain. (b) Scanning electron microscopic image of cathode surface with cells highlighted in yellow.
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from biofilms of Geobacter sulfurreducens comparable to mixed community
17. Reguera, G., K. P. Nevin, J. S. Nicoll, S. F. Covalla, T. L. Woodard, and
D. R. Lovley. 2006. Biofilm and nanowire production leads to increased
current in Geobacter sulfurreducens fuel cells. Appl. Environ. Microbiol.
18. Cord-Ruwisch, R., H. Seitz, and R. Conrad. 1988. The capacity of
hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen
depends on the redox potential of the terminal electron acceptor. Arch.
19. Araujo, J. C., F. C. Téran, R. A. Oliveira, E. A. A. Nour, A. P.
Montenegro, J. R. Campos, and R. F. Vazoller. 2003. Comparison of
of anaerobic biofilms and granular sludge. J. Electron Microsc. 52:
20. JASON, Mitre Corporation. 2006. Engineering microorganisms for en-
ergy production. Department of Energy Report JSR-05-300. JASON, Mi-
tre Corporation, McLean, VA.
21. Fortman, J. L., S. Chhabra, A. Mukhopadhyay, H. Chou, T. S. Lee, E.
Steen, and J. D. Keasling. 2008. Biofuel alternatives to ethanol: pumping
the microbial well. Trends Biotechnol. 26:375–381.
22. Yan, Y., and J. C. Liao. 2009. Engineering metabolic systems for the
production of advanced fuels. J. Ind. Microbiol. Biotechnol. 36:471–479.
23. Kopke, M. 2009. Genetische Veranderung von Clostridium ljungdahlii
zur Produktion von 1-butanol aus Synthesegas. Ph.D. Dissertation. Ulm
University, Hamburg, Germany.
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