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Energetic and Molecular Constraints on the Mechanism of Environmental Fe(III) Reduction by Geobacter

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Microbial Metal Respiration

Abstract

This review aims to discuss how Geobacter and its relatives are shaped by the nature of their electron donor and acceptor, where electrons liberated during complete cytoplasmic oxidation of organics must travel far beyond the cell to reduce extracellular metals without the aid of soluble shuttles. This sequence of reactions must often occur in permanently anoxic habitats where reactant concentrations lower the ∆G to only tens of kJ/mol, severely limiting the energy available for protein synthesis. Extracellular Fe(III) reduction is additionally challenging, from a bioenergetic perspective, as oxidation of organic matter (releasing protons and electrons) occurs in the cell interior, but only the negatively charged electrons are transferred outside the cell. Finally, the low amount of energy available from metals in direct contact with a cell predicts that Geobacter must organize electron transfer proteins to extend outward, to take advantage of the Fe(III) in the volume available a few microns beyond its outer membrane. This review will discuss these thermodynamic constraints on environmental metal reduction, and briefly mention recently described aspects of the molecular mechanism of electron transfer by Geobacter spp. when viewed through this lens.

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References

  • Afkar E, Reguera G, Schiffer M, Lovley DR (2005) A novel Geobacteraceae-specific outer membrane protein J (OmpJ) is essential for electron transport to Fe(III) and Mn(IV) oxides in Geobacter sulfurreducens. BMC Microbiol 5:41

    PubMed  Google Scholar 

  • Aklujkar M, Krushkal J, DiBartolo G, Lapidus A, Land ML, Lovley DR (2009) The genome sequence of Geobacter metallireducens: features of metabolism, physiology and regulation common and dissimilar to Geobacter sulfurreducens. BMC Microbiol 9:109

    PubMed  Google Scholar 

  • Aklujkar M, Young ND, Holmes D, Chavan M, Risso C, Kiss HE, Han CS, Land ML, Lovley DR (2010) The genome of Geobacter bemidjiensis, exemplar for the subsurface clade of Geobacter species that predominate in Fe(III)-reducing subsurface environments. BMC Genomics 11:490

    PubMed  Google Scholar 

  • Anderson RT, Lovley DR (1997) Ecology and biogeochemistry of in situ groundwater bioremediation. Adv Microbial Ecol 15:289–350

    CAS  Google Scholar 

  • Anderson RT, Lovley DR (1999) Naphthalene and benzene degradation under Fe(III)-reducing conditions in petroleum-contaminated aquifers. Bioremediation J 3:121–135

    CAS  Google Scholar 

  • Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485

    PubMed  CAS  Google Scholar 

  • Butler JE, Kaufmann F, Coppi MV, Núñez C, Lovley DR (2004) MacA, a diheme c-type cytochrome involved in Fe(III) reduction by Geobacter sulfurreducens. J Bacteriol 186:4042–4045

    PubMed  CAS  Google Scholar 

  • Butler JE, Young ND, Lovley DR (2009) Evolution from a respiratory ancestor to fill syntrophic and fermentative niches: comparative fenomics of six Geobacteraceae species. BMC Genomics 10:103

    PubMed  Google Scholar 

  • Butler JE, Young ND, Lovley DR (2010) Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11:40

    PubMed  Google Scholar 

  • Callister SJ, Wilkins MJ, Nicora CD, Williams KH, Banfield JF, VerBerkmoes NC, Hettich RL, N’Guessan L, Mouser PJ, Elifantz H, Smith RD, Lovley DR, Lipton MS, Long PE (2010) Analysis of biostimulated microbial communities from two field experiments reveals temporal and spatial differences in proteome profiles. Environ Sci Technol 44:8897–8903

    PubMed  CAS  Google Scholar 

  • Chae K-J, Choi M-J, Lee J-W, Kim K-Y, Kim IS (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Bioresour Technol 100:3518–3525

    PubMed  CAS  Google Scholar 

  • Chang YJ, Long PE, Geyer R, Peacock AD, Resch CT, Sublette K, Pfiffner S, Smithgall A, Anderson RT, Vrionis HA, Stephen JR, Dayvault R, Ortiz-Bernad I, Lovley DR, White DC (2005) Microbial incorporation of 13C-labeled acetate at the field scale: detection of microbes responsible for reduction of U(VI). Environ Sci Technol 39:9039–9048

    PubMed  CAS  Google Scholar 

  • Chin KJ, Esteve-Nunez A, Leang C, Lovley DR (2004) Direct correlation between rates of anaerobic respiration and levels of mRNA for key respiratory genes in Geobacter sulfurreducens. Appl Environ Microbiol 70:5183–5189

    PubMed  CAS  Google Scholar 

  • Coates JD, Bhupathiraju VK, Achenbach LA, McInerney MJ, Lovley DR (2001) Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 51:581–588

    PubMed  CAS  Google Scholar 

  • Coates JD, Ellis DJ, Blunt-Harris EL, Gaw CV, Roden EE, Lovley DR (1998) Recovery of humic-reducing bacteria from a diversity of environments. Appl Environ Microbiol 64:1504–1509

    PubMed  CAS  Google Scholar 

  • Coates JD, Lonergan DJ, Philips EJ, Jenter H, Lovley DR (1995) Desulfuromonas palmitatis sp. nov., a marine dissimilatory Fe(III) reducer that can oxidize long-chain fatty acids. Arch Microbiol 164:406–413

    PubMed  CAS  Google Scholar 

  • Coates JD, Phillips EJ, Lonergan DJ, Jenter H, Lovley DR (1996) Isolation of Geobacter species from diverse sedimentary environments. Appl Environ Microbiol 62:1531–1536

    PubMed  CAS  Google Scholar 

  • Cologgi DL, Lampa-Pastirk S, Speers AM, Kelly SD, Reguera G (2011) Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc Natl Acad Sci U S A 108:15248–15252

    PubMed  CAS  Google Scholar 

  • Coursolle D, Baron DB, Bond DR, Gralnick JA (2010) The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J Bacteriol 192:467–474

    PubMed  CAS  Google Scholar 

  • Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77:995–1008

    CAS  Google Scholar 

  • de Cárcer DA, Ha PT, Jang JK, Chang IS (2011) Microbial community differences between propionate-fed microbial fuel cell systems under open and closed circuit conditions. Appl Microbiol Biotechnol 89:605–612

    PubMed  Google Scholar 

  • Denef VJ, Kalnejais LH, Mueller RS, Wilmes P, Baker BJ, Thomas BC, VerBerkmoes NC, Hettich RL, Banfield JF (2010a) Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc Natl Acad Sci U S A 107:2383–2390

    PubMed  CAS  Google Scholar 

  • Denef VJ, Mueller RS, Banfield JF (2010b) AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4:599–610

    PubMed  Google Scholar 

  • Ding YH, Hixson KK, Aklujkar MA, Lipton MS, Smith RD, Lovley DR, Mester T (2008) Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor. Biochim Biophys Acta 1784:1935–1941

    PubMed  CAS  Google Scholar 

  • Ding YHR, Hixson KK, Giometti CS, Stanley A, Esteve-Nunez A, Khare T, Tollaksen SL, Zhu WH, Adkins JN, Lipton MS, Smith RD, Mester T, Lovley DR (2006) The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions. BBA-Prot Proteomics 1764:1198–1206

    CAS  Google Scholar 

  • Elifantz H, N’Guessan LA, Mouser PJ, Williams KH, Wilkins MJ, Risso C, Holmes DE, Long PE, Lovley DR (2010) Expression of acetate permease-like (apl) genes in subsurface communities of Geobacter species under fluctuating acetate concentrations. FEMS Microbiol Ecol 73:441–449

    PubMed  CAS  Google Scholar 

  • Erickson HP (2009) Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol Proced 11:32–51

    CAS  Google Scholar 

  • Esteve-Nunez A, Rothermich M, Sharma M, Lovley D (2005) Growth of Geobacter sulfurreducens under nutrient-limiting conditions in continuous culture. Environ Microbiol 7:641–648

    PubMed  CAS  Google Scholar 

  • Finkelstein DA, Tender LM, Zeikus JG (2006) Effect of electrode potential on electrode-reducing microbiota. Environ Sci Technol 40:6990–6995

    PubMed  CAS  Google Scholar 

  • Gebhardt NA, Thauer RK, Linder D, Kaulfers PM, Pfennig N (1985) Mechanism of acefate oxidation of CO2 with elemental sulfur in Desulfuromonas acetoxidans. Arch Microbiol 141:392–398

    CAS  Google Scholar 

  • Gray HB, Winkler JR (2010) Electron flow through metalloproteins. Biochimica Et Biophysica Acta-Bioenergetics 1797:1563–1572

    CAS  Google Scholar 

  • Gray HB, Winkler JR (2009) Electron flow through proteins. Chem Phys Lett 483:1–9

    PubMed  CAS  Google Scholar 

  • Ha PT, Tae B, Chang IS (2008) Performance and bacterial consortium of microbial fuel cell fed with formate. Energy Fuels 22:164–168

    CAS  Google Scholar 

  • Hager AJ, Bolton DL, Pelletier MR, Brittnacher MJ, Gallagher LA, Kaul R, Skerrett SJ, Miller SI, Guina T (2006) Type IV pili-mediated secretion modulates Francisella virulence. Mol Microbiol 62:227–237

    PubMed  CAS  Google Scholar 

  • Hartshorne RS, Reardon CL, Ross D, Nuester J, Clarke TA, Gates AJ, Mills PC, Fredrickson JK, Zachara JM, Shi L, Beliaev AS, Marshall MJ, Tien M, Brantley S, Butt JN, Richardson DJ (2009) Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci U S A 106:22169–22174

    PubMed  CAS  Google Scholar 

  • Holmes DE, Bond DR, O’Neil RA, Reimers CE, Tender LR, Lovley DR (2004a) Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microbial Ecol 48:178–190

    CAS  Google Scholar 

  • Holmes DE, Mester T, O’Neil RA, Perpetua LA, Larrahondo MJ, Glaven R, Sharma ML, Ward JE, Nevin KP, Lovley DR (2008a) Genes for two multicopper proteins required for Fe(III) oxide reduction in Geobacter sulfurreducens have different expression patterns both in the subsurface and on energy-harvesting electrodes. Microbiology 154:1422–1435

    PubMed  CAS  Google Scholar 

  • Holmes DE, Nevin KP, Lovley DR (2004b) Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov. Int J Syst Evol Microbiol 54:1591–1599

    PubMed  CAS  Google Scholar 

  • Holmes DE, Nicoll JS, Bond DR, Lovley DR (2004c) Potential role of a novel psychrotolerant member of the family Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov, sp. nov., in electricity production by a marine sediment fuel cell. Appl Environ Microbiol 70:6023–6030

    PubMed  CAS  Google Scholar 

  • Holmes DE, O’Neil RA, Chavan MA, N’guessan LA, Vrionis HA, Perpetua LA, Larrahondo MJ, Didonato R, Liu A, Lovley DR (2009) Transcriptome of Geobacter uraniireducens growing in uranium-contaminated subsurface sediments. Isme J 3:216–230

    Google Scholar 

  • Holmes DE, O’Neil RA, Vrionis HA, N’Guessan LA, Ortiz-Bernad I, Larrahondo MJ, Adams LA, Ward JA, Nicoll JS, Nevin KP, Chavan MA, Johnson JP, Long PE, Lovley DR (2007) Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J 1:663–677

    PubMed  CAS  Google Scholar 

  • Inoue K, Leang C, Franks AE, Woodard TL, Nevin KP, Lovley DR (2011) Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens. Environ Microbiol Rep 3:211–217

    CAS  Google Scholar 

  • Inoue K, Qian X, Morgado L, Kim B-C, Mester T, Izallalen M, Salgueiro CA, Lovley DR (2010) Purification and characterization of OmcZ, an outer-surface, octaheme c-type cytochrome essential for optimal current production by Geobacter sulfurreducens. Appl Environ Microbiol 76:3999–4007

    PubMed  CAS  Google Scholar 

  • Jain A, Gazzola G, Panzera A, Zanoni M, Marsili E (2011) Visible spectroelectrochemical characterization of Geobacter sulfurreducens biofilms on optically transparent indium tin oxide electrode. Electrochim Acta 56:10776–10785

    Google Scholar 

  • Juarez K, Kim BC, Nevin K, Olvera L, Reguera G, Lovley DR, Methe BA (2009) PilR, a transcriptional regulator for pilin and other genes required for Fe(III) reduction in Geobacter sulfurreducens. J Mol Microbiol Biotechnol 16:146–158

    PubMed  CAS  Google Scholar 

  • Jung S, Regan JM (2007) Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors. Appl Microbiol Biotechnol 77:393–402

    PubMed  CAS  Google Scholar 

  • Kashefi K, Holmes DE, Baross JA, Lovley DR (2003) Thermophily in the Geobacteraceae: Geothermobacter ehrlichii gen. nov., sp. nov., a novel thermophilic member of the Geobacteraceae from the “Bag City” hydrothermal vent. Appl Environ Microbiol 69:2985–2993

    PubMed  CAS  Google Scholar 

  • Kerisit S, Rosso KM, Dupuis M, Valiev M (2007) Molecular computational investigation of electron-transfer kinetics across cytochrome-iron oxide interfaces. J Phys Chem C 111:11363–11375

    CAS  Google Scholar 

  • Kiely PD, Cusick R, Call DF, Selembo PA, Regan JM, Logan BE (2011) Anode microbial communities produced by changing from microbial fuel cell to microbial electrolysis cell operation using two different wastewaters. Bioresour Technol 102:388–394

    PubMed  CAS  Google Scholar 

  • Kim BC, Leang C, Ding YH, Glaven RH, Coppi MV, Lovley DR (2005) OmcF, a putative c-Type monoheme outer membrane cytochrome required for the expression of other outer membrane cytochromes in Geobacter sulfurreducens. J Bacteriol 187:4505–4513

    PubMed  CAS  Google Scholar 

  • Kim BC, Lovley DR (2008) Investigation of direct vs. indirect involvement of the c-type cytochrome MacA in Fe(III) reduction by Geobacter sulfurreducens. FEMS Microbiol Lett 286:39–44

    PubMed  CAS  Google Scholar 

  • Kim BC, Postier BL, DiDonato RJ, Chaudhuri SK, Nevin KP, Lovley DR (2008) Insights into genes involved in electricity generation in Geobacter sulfurreducens via whole genome microarray analysis of the OmcF-deficient mutant. Bioelectrochemistry 73:70–75

    PubMed  CAS  Google Scholar 

  • Kim BC, Qian XL, Ching LA, Coppi MV, Lovley DR (2006) Two putative c-type multiheme cytochromes required for the expression of OmcB, an outer membrane protein essential for optimal Fe(III) reduction in Geobacter sulfurreducens. J Bacteriol 188:3138–3142

    PubMed  CAS  Google Scholar 

  • King GM, Klug MJ, Lovley DR (1983) Metabolism of acetate, methanol, and methylated amines in intertidal sediments of Lowes Cove, Maine. Appl Environ Microbiol 45:1848–1853

    PubMed  CAS  Google Scholar 

  • Klimes A, Franks AE, Glaven RH, Tran H, Barrett CL, Qiu Y, Zengler K, Lovley DR (2010) Production of pilus-like filaments in Geobacter sulfurreducens in the absence of the type IV pilin protein PilA. FEMS Microbiol Lett 310:62–68

    PubMed  CAS  Google Scholar 

  • Krushkal J, Juarez K, Barbe JF, Qu Y, Andrade A, Puljic M, Adkins RM, Lovley DR, Ueki T (2010) Genome-wide survey for PilR recognition sites of the metal-reducing prokaryote Geobacter sulfurreducens. Gene 469:31–44

    PubMed  CAS  Google Scholar 

  • Leang C, Adams LA, Chin KJ, Nevin KP, Methe BA, Webster J, Sharma ML, Lovley DR (2005) Adaptation to disruption of the electron transfer pathway for Fe(III) reduction in Geobacter sulfurreducens. J Bacteriol 187:5918–5926

    PubMed  CAS  Google Scholar 

  • Leang C, Coppi MV, Lovley DR (2003) OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J Bacteriol 185:2096–2103

    PubMed  CAS  Google Scholar 

  • Leang C, Lovley DR (2005) Regulation of two highly similar genes, omcB and omcC, in a 10 kb chromosomal duplication in Geobacter sulfurreducens. Microbiology 151:1761–1767

    PubMed  CAS  Google Scholar 

  • Leang C, Qian X, Mester T, Lovley DR (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl Environ Microbiol 76:4080–4084

    PubMed  CAS  Google Scholar 

  • Lin B, Braster M, Roling WFM, van Breukelen BM (2007) Iron-reducing microorganisms in a landfill leachate-polluted aquifer: complementing culture-independent information with enrichments and isolations. Geomicrobiol J 24:283–294

    CAS  Google Scholar 

  • Lloyd JR, Leang C, Hodges Myerson AL, Coppi MV, Cuifo S, Methe B, Sandler SJ, Lovley DR (2003) Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem J 369:153–161

    PubMed  CAS  Google Scholar 

  • Lonergan DJ, Jenter HL, Coates JD, Phillips EJP, Schmidt TM, Lovley DR (1996) Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria. J Bacteriol 178:2402–2408

    PubMed  CAS  Google Scholar 

  • Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:35–44

    PubMed  CAS  Google Scholar 

  • Lovley DR, Anderson RT (2000) Influence of dissimilatory metal reduction on fate of organic and metal contaminants in the subsurface. Hydrogeology J 8:77–88

    CAS  Google Scholar 

  • Lovley DR, Klug MJ (1982) Intermediary metabolism of organic matter in the sediments of a eutrophic lake. Appl Environ Microbiol 43:552–560

    PubMed  CAS  Google Scholar 

  • Magnuson TS, Hodges-Myerson AL, Lovley DR (2000) Characterization of a membrane-bound NADH-dependent Fe3+ reductase from the dissimilatory Fe3+-reducing bacterium Geobacter sulfurreducens. FEMS Microbiol Lett 185:205–211

    PubMed  CAS  Google Scholar 

  • Magnuson TS, Isoyama N, Hodges-Myerson AL, Davidson G, Maroney MJ, Geesey GG, Lovley DR (2001) Isolation, characterization and gene sequence analysis of a membrane-associated 89 kDa Fe(III) reducing cytochrome c from Geobacter sulfurreducens. Biochem J 359:147–152

    PubMed  CAS  Google Scholar 

  • Mahadevan R, Bond DR, Butler JE, Esteve-Nunez A, Coppi MV, Palsson BO, Schilling CH, Lovley DR (2006) Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. Appl Environ Microbiol 72:1558–1568

    PubMed  CAS  Google Scholar 

  • Mahadevan R, Palsson BO, Lovley DR (2011) In situ to in silico and back: elucidating the physiology and ecology of Geobacter spp. using genome-scale modelling. Nat Rev Microbiol 9:39–50

    PubMed  CAS  Google Scholar 

  • Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008a) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105:3968–3973

    PubMed  CAS  Google Scholar 

  • Marsili E, Rollefson JB, Baron DB, Hozalski RM, Bond DR (2008b) Microbial biofilm voltammetry: direct electrochemical characterization of catalytic electrode-attached biofilms. Appl Environ Microbiol 74:7329–7337

    PubMed  CAS  Google Scholar 

  • Marsili E, Sun J, Bond DR (2010) Voltammetry and growth physiology of Geobacter sulfurreducens biofilms as a function of growth stage and imposed electrode potential. Electroanalysis 22:865–874

    CAS  Google Scholar 

  • Mehta T, Childers SE, Glaven R, Lovley DR, Mester T (2006) A putative multicopper protein secreted by an atypical type II secretion system involved in the reduction of insoluble electron acceptors in Geobacter sulfurreducens. Microbiology 152:2257–2264

    PubMed  CAS  Google Scholar 

  • Mehta T, Coppi MV, Childers SE, Lovley DR (2005) Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol 71:8634–8641

    PubMed  CAS  Google Scholar 

  • Methe BA, Nelson KE, Eisen JA, Paulsen IT, Nelson W, Heidelberg JF, Wu D, Wu M, Ward N, Beanan MJ, Dodson RJ, Madupu R, Brinkac LM, Daugherty SC, DeBoy RT, Durkin AS, Gwinn M, Kolonay JF, Sullivan SA, Haft DH, Selengut J, Davidsen TM, Zafar N, White O, Tran B, Romero C, Forberger HA, Weidman J, Khouri H, Feldblyum TV, Utterback TR, Van Aken SE, Lovley DR, Fraser CM (2003) Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302:1967–1969

    PubMed  CAS  Google Scholar 

  • Morita M, Malvankar NS, Franks AE, Summers ZM, Giloteaux L, Rotaru AE, Rotaru C, Lovley DR (2011) Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates mBio 2:e00159-00111

    Google Scholar 

  • Nagarajan H, Butler JE, Klimes A, Qiu Y, Zengler K, Ward J, Young ND, Methé BA, Palsson BØ, Lovley DR, Barrett CL (2010) De novo assembly of the complete genome of an enhanced electricity-producing variant of Geobacter sulfurreducens using only short reads. PLoS One 5:e10922

    PubMed  Google Scholar 

  • Nevin KP, Holmes DE, Woodard TL, Hinlein ES, Ostendorf DW, Lovley DR (2005) Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates. Int J Syst Evol Microbiol 55:1667–1674

    PubMed  CAS  Google Scholar 

  • Nevin KP, Kim BC, Glaven RH, Johnson JP, Woodard TL, Methe BA, Didonato RJ, Covalla SF, Franks AE, Liu A, Lovley DR (2009) Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One 4:e5628

    PubMed  Google Scholar 

  • Novelli PC, Michelson AR, Scranton MI, Banta GT, Hobbie JE, Howarth RW (1988) Hydrogen and acetate cycling in two sulfate-reducing sediments: Buzzards Bay and Town Cove. Mass Geochim Cosmochim Acta 52:2477–2486

    CAS  Google Scholar 

  • Nunez C, Esteve-Nunez A, Giometti C, Tollaksen S, Khare T, Lin W, Lovley DR, Methe BA (2006) DNA microarray and proteomic analyses of the RpoS regulon in Geobacter sulfurreducens. J Bacteriol 188:2792–2800

    PubMed  CAS  Google Scholar 

  • Paulsen J, Kroger A, Thauer RK (1986) ATP-driven succinate oxidation in the catabolism of Desulfuromonas acetoxidans. Arch Microbiol 144:78–83

    CAS  Google Scholar 

  • Petrie L, North NN, Dollhopf SL, Balkwill DL, Kostka JE (2003) Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI). Appl Environ Microbiol 69:7467–7479

    PubMed  CAS  Google Scholar 

  • Pfennig N, Biebl H (1976) Desulfuromonas acetoxidans gen. nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium. Arch Microbiol 110:3–12

    PubMed  CAS  Google Scholar 

  • Pfennig N, Widdel F (1982) The bacteria of the sulphur cycle. Philos Trans R Soc Lond B Biol Sci 298:433–441

    PubMed  CAS  Google Scholar 

  • Qian X, Reguera G, Mester T, Lovley DR (2007) Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins. FEMS Microbiol Lett 277:21–27

    PubMed  CAS  Google Scholar 

  • Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    PubMed  CAS  Google Scholar 

  • Reguera G, Nevin KP, Nicoll JS, Covalla SF, Woodard TL, Lovley DR (2006) Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 72:7345–7348

    PubMed  CAS  Google Scholar 

  • Richter H, Nevin KP, Jia HF, Lowy DA, Lovley DR, Tender LM (2009) Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer. Energy Environ Sci 2:506–516

    CAS  Google Scholar 

  • Richter LV, Sandler SJ, Weis RM (2012) Two isoforms of the Geobacter sulfurreducens PilA have distinct roles in pilus biogenesis, cytochrome localization, extracellular electron transfer and biofilm formation. J Bacteriol 194(10):2551–2563

    Google Scholar 

  • Rodrigues JLM, Serres MH, Tiedje JM (2011) Large-scale comparative phenotypic and genomic analyses reveal ecological preferences of shewanella species and identify metabolic pathways conserved at the genus level. Appl Environ Microbiol 77:5352–5360

    PubMed  CAS  Google Scholar 

  • Rollefson JB, Levar CE, Bond DR (2009) Identification of genes involved in biofilm formation and respiration via mini-Himar transposon mutagenesis of Geobacter sulfurreducens. J Bacteriol 191:4207–4217

    PubMed  CAS  Google Scholar 

  • Rollefson JB, Stephen CS, Tien M, Bond DR (2011) Identification of an extracellular polysaccharide network essential for cytochrome anchoring and biofilm formation in Geobacter sulfurreducens. J Bacteriol 193:1023–1033

    PubMed  CAS  Google Scholar 

  • Rooney-Varga JN, Anderson RT, Fraga JL, Ringelberg D, Lovley DR (1999) Microbial communities associated with anaerobic benzene mineralization in a petroleum-contaminated aquifer. Appl Environ Microbiol 65:3056–3063

    PubMed  CAS  Google Scholar 

  • Ross DE, Brantley SL, Tien M (2009) Kinetic characterization of terminal reductases OmcA and MtrC involved in respiratory electron transfer for dissimilatory iron reduction in Shewanella oneidensis MR-1. Appl Environ Microbiol 75:5218–5226

    PubMed  CAS  Google Scholar 

  • Schmitz RA, Bonch-Osmolovskaya EA, Thauer RK (1990) Different mechanisms of acetate activation in Desulfurella acetivorans and Desulfuromonas acetooxidans. Arch Microbiol 154:274–279

    CAS  Google Scholar 

  • Seidel JM, Hoffmann KE, Ellis A, Seidel T, Spatzal S, Gerhardt SJ, Elliott, Einsle O (2012) MacA is a second Cytochrome c peroxidase of Geobacter sulfurreducens. Biochemistry 51:2747–2756

    Google Scholar 

  • Shelobolina ES, Coppi MV, Korenevsky AA, DiDonato LN, Sullivan SA, Konishi H, Xu H, Leang C, Butler JE, Kim BC, Lovley DR (2007) Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BMC Microbiol 7:16

    PubMed  Google Scholar 

  • Snoeyenbos-West OL, Nevin KP, Anderson RT, Lovley DR (2000) Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microbial Ecol 39:153–167

    CAS  Google Scholar 

  • Srikanth S, Marsili E, Flickinger MC, Bond DR (2008) Electrochemical characterization of Geobacter sulfurreducens cells immobilized on graphite paper electrodes. Biotechnol Bioeng 99:1065–1073

    PubMed  CAS  Google Scholar 

  • Straub KL, Benz M, Schink B (2001) Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol Ecol 34:181–186

    PubMed  CAS  Google Scholar 

  • Straub KL, Hanzlik M, Buchholz-Cleven BE (1998) The use of biologically produced ferrihydrite for the isolation of novel iron-reducing bacteria. Syst Appl Microbiol 21:442–449

    PubMed  CAS  Google Scholar 

  • Strycharz SM, Malanoski AP, Snider RM, Yi H, Lovley DR, Tender LM (2011) Application of cyclic voltammetry to investigate enhanced catalytic current generation by biofilm-modified anodes of Geobacter sulfurreducens strain DL1 vs. variant strain KN400. Energy Environ Sci 4:896–913

    CAS  Google Scholar 

  • Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM (2011) On the electrical conductivity of microbial nanowires and biofilms. Energy Environ Sci 4:4366–4379

    CAS  Google Scholar 

  • Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330:1413–1415

    PubMed  CAS  Google Scholar 

  • Sun J, Sayyar B, Butler JE, Pharkya P, Fahland TR, Famili I, Schilling CH, Lovley DR, Mahadevan R (2009) Genome-scale constraint-based modeling of Geobacter metallireducens. BMC Syst Biol 3:15

    PubMed  Google Scholar 

  • Thauer RK, Moller-Zinkhan D, Spormann AM (1989) Biochemistry of acetate catabolism in anaerobic chemotrophic bacteria. Ann Rev Microbiol 43:43–67

    CAS  Google Scholar 

  • Tran HT, Krushkal J, Antommattei FM, Lovley DR, Weis RM (2008) Comparative genomics of Geobacter chemotaxis genes reveals diverse signaling function. BMC Genomics 9:471–486

    PubMed  Google Scholar 

  • von Canstein H, Ogawa J, Shimizu S, Lloyd JR (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74:615–623

    Google Scholar 

  • Vrionis HA, Anderson RT, Ortiz-Bernad I, O’Neill KR, Resch CT, Peacock AD, Dayvault R, White DC, Long PE, Lovley DR (2005) Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site. Appl Environ Microbiol 71:6308–6318

    PubMed  CAS  Google Scholar 

  • Widdel F, Pfennig N (1992) The genus Desulfuromonas and other gram-negative sulfur-reducing eubacteria. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes, vol IV. Springer-Verlag, New York, pp 3379–3392

    Google Scholar 

  • Wilkins MJ, Callister SJ, Miletto M, Williams KH, Nicora CD, Lovley DR, Long PE, Lipton MS (2011) Development of a biomarker for Geobacter activity and strain composition; proteogenomic analysis of the citrate synthase protein during bioremediation of U(VI). Microb Biotechnol 4:55–63

    PubMed  CAS  Google Scholar 

  • Williams KH, Nevin KP, Franks A, Englert A, Long PE, Lovley DR (2010) Electrode-based approach for monitoring in situ microbial activity during subsurface bioremediation. Environ Sci Technol 44:47–54

    PubMed  CAS  Google Scholar 

  • Xing D, Cheng S, Regan JM, Logan BE (2009) Change in microbial communities in acetate- and glucose-fed microbial fuel cells in the presence of light. Biosens Bioelectron 25:105–111

    PubMed  CAS  Google Scholar 

  • Yang TH, Coppi MV, Lovley DR, Sun J (2010) Metabolic response of Geobacter sulfurreducens towards electron donor/acceptor variation. Microb Cell Fact 9:90

    PubMed  CAS  Google Scholar 

  • Yi H, Nevin KP, Kim BC, Franks AE, Klimes A, Tender LM, Lovley DR (2009) Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens Bioelectron 24:3498–3503

    PubMed  CAS  Google Scholar 

  • Yun J, Ueki T, Miletto M, Lovley DR (2011) Monitoring the metabolic status of Geobacter species in contaminated groundwater by quantifying key metabolic proteins with Geobacter-specific antibodies. Appl Environ Microbiol 77:4597–4602

    PubMed  CAS  Google Scholar 

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Acknowledgments

D. R. B. and C. E. L. and J. B. R. are supported by the Office of Science (BER), U.S. Department of Energy, (DE-SC0006868) and the Office of Naval Research (N000141210308).

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  1. 140 Gortner Laboratory, Department of Microbiology and BioTechnology Institute, University of Minnesota, 1479 Gortner Avenue, St. Paul, Minneapolis, MN, 55108, USA

    C. E. Levar, J. B. Rollefson & D. R. Bond

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  1. C. E. Levar
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  2. J. B. Rollefson
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  3. D. R. Bond
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Correspondence to D. R. Bond .

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  1. Institute for Applied Biosciences, Karlsruhe Institute of Technology, Fritz-Haber-Weg 2, Karlsruhe, 76131, Germany

    Johannes Gescher

  2. , Center for Applied Geoscience (ZAG), Geo, Eberhard-Karls-University Tuebingen, Sigwartstrasse 10, Tuebingen, 72076, Germany

    Andreas Kappler

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Levar, C.E., Rollefson, J.B., Bond, D.R. (2013). Energetic and Molecular Constraints on the Mechanism of Environmental Fe(III) Reduction by Geobacter . In: Gescher, J., Kappler, A. (eds) Microbial Metal Respiration. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32867-1_2

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