Electricity Production by Geobacter sulfurreducens Attached to Electrodes

ABSTRACT Previous studies have suggested that members of the Geobacteraceae can use electrodes as electron acceptors for anaerobic respiration. In order to better understand this electron transfer process for energy production, Geobacter sulfurreducens was inoculated into chambers in which a graphite electrode served as the sole electron acceptor and acetate or hydrogen was the electron donor. The electron-accepting electrodes were maintained at oxidizing potentials by connecting them to similar electrodes in oxygenated medium (fuel cells) or to potentiostats that poised electrodes at +0.2 V versus an Ag/AgCl reference electrode (poised potential). When a small inoculum of G. sulfurreducens was introduced into electrode-containing chambers, electrical current production was dependent upon oxidation of acetate to carbon dioxide and increased exponentially, indicating for the first time that electrode reduction supported the growth of this organism. When the medium was replaced with an anaerobic buffer lacking nutrients required for growth, acetate-dependent electrical current production was unaffected and cells attached to these electrodes continued to generate electrical current for weeks. This represents the first report of microbial electricity production solely by cells attached to an electrode. Electrode-attached cells completely oxidized acetate to levels below detection (<10 μM), and hydrogen was metabolized to a threshold of 3 Pa. The rates of electron transfer to electrodes (0.21 to 1.2 μmol of electrons/mg of protein/min) were similar to those observed for respiration with Fe(III) citrate as the electron acceptor (Eo′ =+0.37 V). The production of current in microbial fuel cell (65 mA/m2 of electrode surface) or poised-potential (163 to 1,143 mA/m2) mode was greater than what has been reported for other microbial systems, even those that employed higher cell densities and electron-shuttling compounds. Since acetate was completely oxidized, the efficiency of conversion of organic electron donor to electricity was significantly higher than in previously described microbial fuel cells. These results suggest that the effectiveness of microbial fuel cells can be increased with organisms such as G. sulfurreducens that can attach to electrodes and remain viable for long periods of time while completely oxidizing organic substrates with quantitative transfer of electrons to an electrode.

[1]  L. B. Wingard,et al.  Bioelectrochemical fuel cells , 1982 .

[2]  D. Lovley,et al.  Organic Matter Mineralization with Reduction of Ferric Iron in Anaerobic Sediments , 1986, Applied and environmental microbiology.

[3]  D. Lovley,et al.  Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments , 1988 .

[4]  D. Lovley,et al.  Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese , 1988, Applied and environmental microbiology.

[5]  Bernhard Schink,et al.  Enhanced Propionate Formation by Propionibacterium freudenreichii subsp. freudenreichii in a Three-Electrode Amperometric Culture System , 1990, Applied and environmental microbiology.

[6]  T. Schmidt,et al.  Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria , 1996, Journal of bacteriology.

[7]  D. Lovley,et al.  Growth of Geobacter sulfurreducens with Acetate in Syntrophic Cooperation with Hydrogen-Oxidizing Anaerobic Partners , 1998, Applied and Environmental Microbiology.

[8]  Byung Hong Kim,et al.  Direct electrode reaction of Fe(III)-reducing bacterium, Shewanella putrefaciens , 1999 .

[9]  S. Chaturvedi,et al.  Protein S Deficiency, Activated Protein C Resistance and Sticky Platelet Syndrome in a Young Woman with Bilateral Strokes , 1999, Cerebrovascular Diseases.

[10]  Derek R. Lovley,et al.  Lack of Production of Electron-Shuttling Compounds or Solubilization of Fe(III) during Reduction of Insoluble Fe(III) Oxide by Geobacter metallireducens , 2000, Applied and Environmental Microbiology.

[11]  D. Lovley,et al.  Characterization of a membrane-bound NADH-dependent Fe(3+) reductase from the dissimilatory Fe(3+)-reducing bacterium Geobacter sulfurreducens. , 2000, FEMS microbiology letters.

[12]  Y. Choi,et al.  Effect of initial carbon sources on the performance of microbial fuel cells containing Proteus vulgaris. , 2000, Biotechnology and bioengineering.

[13]  D. Park,et al.  Electricity Generation in Microbial Fuel Cells Using Neutral Red as an Electronophore , 2000, Applied and Environmental Microbiology.

[14]  Dianne K. Newman,et al.  A role for excreted quinones in extracellular electron transfer , 2000, Nature.

[15]  L. Tender,et al.  Harvesting Energy from the Marine Sediment−Water Interface , 2001 .

[16]  D. Lovley,et al.  Isolation, characterization and gene sequence analysis of a membrane-associated 89 kDa Fe(III) reducing cytochrome c from Geobacter sulfurreducens. , 2001, The Biochemical journal.

[17]  Byung Hong Kim,et al.  A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Clostridium butyricum isolated from a microbial fuel cell , 2001 .

[18]  Seunho Jung,et al.  Optimization of the performance of microbial fuel cells containing alkalophilic Bacillus sp. , 2001 .

[19]  Comas Haynes,et al.  Clarifying reversible efficiency misconceptions of high temperature fuel cells in relation to reversible heat engines , 2001 .

[20]  C. Leang,et al.  Development of a Genetic System forGeobacter sulfurreducens , 2001, Applied and Environmental Microbiology.

[21]  L. Tender,et al.  Harvesting energy from the marine sediment--water interface. , 2008, Environmental science & technology.

[22]  D. Lowy,et al.  Harnessing microbially generated power on the seafloor , 2002, Nature Biotechnology.

[23]  Derek R. Lovley,et al.  Geobacter metallireducens accesses insoluble Fe(iii) oxide by chemotaxis , 2002, Nature.

[24]  Kelly P. Nevin,et al.  Mechanisms for Fe(III) Oxide Reduction in Sedimentary Environments , 2002 .

[25]  Byung Hong Kim,et al.  A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens , 2002 .

[26]  Kelly P. Nevin,et al.  Mechanisms for Accessing Insoluble Fe(III) Oxide during Dissimilatory Fe(III) Reduction by Geothrix fermentans , 2002, Applied and Environmental Microbiology.

[27]  D. R. Bond,et al.  Electrode-Reducing Microorganisms That Harvest Energy from Marine Sediments , 2002, Science.

[28]  C. Leang,et al.  OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens , 2003, Journal of bacteriology.

[29]  Bernhard Schink,et al.  Anaerobic oxidation of glycerol by Escherichia coli in an amperometric poised-potential culture system , 1989, Applied Microbiology and Biotechnology.

[30]  B. Schink,et al.  Oxidation of glycerol, lactate, and propionate by Propionibacterium freudenreichii in a poised-potential amperometric culture system , 1990, Archives of Microbiology.