Applied Microbiology and Biotechnology

, Volume 98, Issue 20, pp 8481–8495 | Cite as

Electroactive bacteria—molecular mechanisms and genetic tools

  • Anne Sydow
  • Thomas Krieg
  • Florian Mayer
  • Jens Schrader
  • Dirk Holtmann


In nature, different bacteria have evolved strategies to transfer electrons far beyond the cell surface. This electron transfer enables the use of these bacteria in bioelectrochemical systems (BES), such as microbial fuel cells (MFCs) and microbial electrosynthesis (MES). The main feature of electroactive bacteria (EAB) in these applications is the ability to transfer electrons from the microbial cell to an electrode or vice versa instead of the natural redox partner. In general, the application of electroactive organisms in BES offers the opportunity to develop efficient and sustainable processes for the production of energy as well as bulk and fine chemicals, respectively. This review describes and compares key microbiological features of different EAB. Furthermore, it focuses on achievements and future prospects of genetic manipulation for efficient strain development.


Electroactive bacteria (EAB) Bioelectrochemical systems (BES) Genetic tools Strain engineering 

Supplementary material

253_2014_6005_MOESM1_ESM.pdf (343 kb)
ESM 1(PDF 343 kb)


  1. 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 5:41PubMedPubMedCentralGoogle Scholar
  2. 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 9:109PubMedPubMedCentralGoogle Scholar
  3. Alferov S, Coman V, Gustavsson T, Reshetilov A, von Wachenfeldt C, Hägerhäll C, Gorton L (2009) Electrical communication of cytochrome enriched Escherichia coli JM109 cells with graphite electrodes. Electrochim Acta 54:4979–4984Google Scholar
  4. Axe J, Billmyre RB, Duty KH, Hitz G, Trager L, Weatherford A (2009) Harvesting life’s energy: increase in the aerotolerence of the electrogenic anaerobe Geobacter sulfurreducens due to over-expression of superoxide dismutase and catalase.Google Scholar
  5. Baron D, LaBelle E, Coursolle D, Gralnick JA, Bond DR (2009) Electrochemical measurement of electron transfer kinetics by Shewanella oneidensis MR-1. J Biol Chem 284:28865–28873PubMedPubMedCentralGoogle Scholar
  6. Barreto M, Jedlicki E, Holmes DS (2005) Identification of a gene cluster for the formation of extracellular polysaccharide precursors in the chemolithoautotroph Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:2902–2909PubMedPubMedCentralGoogle Scholar
  7. Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555PubMedPubMedCentralGoogle Scholar
  8. Bouhenni R, Gehrke A, Saffarini D (2005) Identification of genes involved in cytochrome c biogenesis in Shewanella oneidensis, using a modified mariner transposon. Appl Environ Microbiol 71:4935–4937PubMedPubMedCentralGoogle Scholar
  9. Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, Culley DE, Reardon CL, Barua S, Romine MF, Zhou J, Beliaev AS, Bouhenni R, Saffarini D, Mansfeld F, Kim BH, Fredrickson JK, Nealson KH (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73:7003–7012PubMedPubMedCentralGoogle Scholar
  10. Bücking C, Schicklberger M, Gescher J (2013) The Biochemistry of Dissimilatory Ferric Iron and Manganese Reduction in Shewanella oneidensis. In: Kappler A, Gescher J (eds) Microbial Metal Respiration. Springer, Verlag Berlin Heidelberg, pp 49–82Google Scholar
  11. Butler JE, Kaufmann F, Coppi MV, Núnez C, Lovley DR (2004) MacA, a diheme c-type cytochrome involved in Fe (III) reduction by Geobacter sulfurreducens. J Bacteriol 186:4042–4045PubMedPubMedCentralGoogle Scholar
  12. Butler JE, Young ND, Lovley DR (2010) Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11:40PubMedPubMedCentralGoogle Scholar
  13. Carbajosa S, Malki M, Caillard R, Lopez MF, Palomares FJ, Martín-Gago JA, Rodríguez N, Amils R, Fernández VM, De Lacey AL (2010) Electrochemical growth of Acidithiobacillus ferrooxidans on a graphite electrode for obtaining a biocathode for direct electrocatalytic reduction of oxygen. Biosens Bioelectron 26:877–880PubMedGoogle Scholar
  14. Cárdenas JP, Valdés J, Quatrini R, Duarte F, Holmes DS (2010) Lessons from the genomes of extremely acidophilic bacteria and archaea with special emphasis on bioleaching microorganisms. Appl Microbiol Biotechnol 88:605–620PubMedGoogle Scholar
  15. Cheng S, Xing D, Call DF, Logan BE (2009) Direct biological conversion of electrical current into methane by electromethanogenesis. Environ Sci Technol 43:3953–3958PubMedGoogle Scholar
  16. Childers SE, Ciufo S, Lovley DR (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416:767–769PubMedGoogle Scholar
  17. Coppi MV, Leang C, Sandler SJ, Lovley DR (2001) Development of a genetic system for Geobacter sulfurreducens. Appl Environ Microbiol 67:3180–3187PubMedPubMedCentralGoogle Scholar
  18. 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 192:467–474PubMedPubMedCentralGoogle Scholar
  19. Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol MicrobiolGoogle Scholar
  20. De Vriendt K, Theunissen S, Carpentier W, De Smet L, Devreese B, Van Beeumen J (2005) Proteomics of Shewanella oneidensis MR-1 biofilm reveals differentially expressed proteins, including AggA and RibB. J Proteome 5:1308–1316Google Scholar
  21. Dolch K, Danzer J, Kabbeck T, Bierer B, Erben J, Förster AH, Maisch J, Nick P, Kerzenmacher S, Gescher J (2014) Characterization of microbial current production as a function of microbe-electrode-interaction. Bioresour Technol 157:284–292PubMedGoogle Scholar
  22. Farah C, Vera M, Morin D, Haras D, Jerez CA, Guiliani N (2005) Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:7033–7040PubMedPubMedCentralGoogle Scholar
  23. Firer-Sherwood M, Pulcu GS, Elliott SJ (2008) Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J Biol Inorg Chem 13:849–854PubMedGoogle Scholar
  24. Firer-Sherwood MA, Bewley KD, Mock J-Y, Elliott SJ (2011) Tools for resolving complexity in the electron transfer networks of multiheme cytochromes c. Metallomics 3:344–348PubMedGoogle Scholar
  25. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL (2008) Towards environmental systems biology of Shewanella. Nature Rev Microbiol 6:592–603Google Scholar
  26. Freguia S, Masuda M, Tsujimura S, Kano K (2009) Lactococcus lactis catalyses electricity generation at microbial fuel cell anodes via excretion of a soluble quinone. Bioelectrochemistry 76:14–18PubMedGoogle Scholar
  27. Gao H, Yang ZK, Wu L, Thompson DK, Zhou J (2006) Global transcriptome analysis of the cold shock response of Shewanella oneidensis MR-1 and mutational analysis of its classical cold shock proteins. J Bacteriol 188:4560–4569PubMedPubMedCentralGoogle Scholar
  28. Girbal L, Vasconcelos I, Saint-Amans S, Soucaille P (1995) How neutral red modified carbon and electron flow in Clostridium acetobutylicum grown in chemostat culture at neutral pH. FEMS Microbiol Rev 16:151–162Google Scholar
  29. Golitsch F, Bücking C, Gescher J (2013) Proof of principle for an engineered microbial biosensor based on Shewanella oneidensis outer membrane protein complexes. Biosens Bioelectron 47:285–291PubMedGoogle Scholar
  30. Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci U S A 103:11358–11363PubMedPubMedCentralGoogle Scholar
  31. Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6:596–604PubMedGoogle Scholar
  32. Hazeu W, Batenburg-van der Vegte WH, Bos P, Pas RK, Kuenen JG (1988) The production and utilization of intermediary elemental sulfur during the oxidation of reduced sulfur compounds by Thiobacillus ferrooxidans. Arch Microbiol 150:574–579Google Scholar
  33. Heap JT, Pennington OJ, Cartman ST, Carter GP, Minton NP (2007) The ClosTron: a universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70:452–464PubMedGoogle Scholar
  34. Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, Eisen JA, Seshadri R, Ward N, Methe B (2002) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol 20:1118–1123PubMedGoogle Scholar
  35. Holmes DE, Chaudhuri SK, Nevin KP, Mehta T, Methé BA, Liu A, Ward JE, Woodard TL, Webster J, Lovley DR (2006) Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ Microbiol 8:1805–1815PubMedGoogle Scholar
  36. Holtmann D, Hannappel A, Schrader J (2014) Microbial electrosynthesis. In: Kreysa G, K-i O, Savinell RF (eds) Encyclopedia of applied electrochemistry. Springer, New York, pp 1268–1275Google Scholar
  37. Kane AL, Bond DR, Gralnick JA (2012) Electrochemical analysis of Shewanella oneidensis engineered to bind gold electrodes. ACS Synth Biol 2:93–101PubMedGoogle Scholar
  38. Kelly DP, Wood AP (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50:511–516PubMedGoogle Scholar
  39. 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 187:4505–4513PubMedPubMedCentralGoogle Scholar
  40. Kim BC, Qian X, Leang C, 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 188:3138–3142PubMedPubMedCentralGoogle Scholar
  41. Kipf E, Koch J, Geiger B, Erben J, Richter K, Gescher J, Zengerle R, Kerzenmacher S (2013) Systematic screening of carbon-based anode materials for microbial fuel cells with Shewanella oneidensis MR-1. Bioresour Technol 146:386–392PubMedGoogle Scholar
  42. Kita A, Iwasaki Y, Sakai S, Okuto S, Takaoka K, Suzuki T, Yano S, Sawayama S, Tajima T, Kato J, Nishio N, Murakami K, Nakashimada Y (2013) Development of genetic transformation and heterologous expression system in carboxydotrophic thermophilic acetogen Moorella thermoacetica. J Biosci Bioeng 115:347–352PubMedGoogle Scholar
  43. Köpke M, Held C, Hujer S, Liesegang H, Wiezer A, Wollherr A, Ehrenreich A, Liebl W, Gottschalk G, Dürre P (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. National Acad Sciences 107:13087–13092Google Scholar
  44. Kouzuma A, Meng X-Y, Kimura N, Hashimoto K, Watanabe K (2010) Disruption of the putative cell surface polysaccharide biosynthesis gene SO3177 in Shewanella oneidensis MR-1 enhances adhesion to electrodes and current generation in microbial fuel cells. Appl Environ Microbiol 76:4151–4157PubMedPubMedCentralGoogle Scholar
  45. Kusano T, Sugawara K, Inoue C, Takeshima T, Numata M, Shiratori T (1992) Electrotransformation of Thiobacillus ferrooxidans with plasmids containing a mer determinant. J Bacteriol 174:6617–6623PubMedPubMedCentralGoogle Scholar
  46. Leang C, Adams LA, Chin K-J, Nevin KP, Methe B, Webster J, Sharma ML, Lovley D (2005) Adaptation to disruption of the electron transfer pathway for Fe (III) reduction in Geobacter sulfurreducens. J Bacteriol 187:5918–5926PubMedPubMedCentralGoogle Scholar
  47. Leang C, Coppi MV, Lovley D (2003) OmcB, a c-type polyheme cytochrome, involved in Fe (III) reduction in Geobacter sulfurreducens. J Bacteriol 185:2096–2103PubMedPubMedCentralGoogle Scholar
  48. Leang C, Lovley DR (2005) Regulation of two highly similar genes, omcB and omcC, in a 10 kb chromosomal duplication in Geobacter sulfurreducens. Microbiology 151:1761–1767PubMedGoogle Scholar
  49. Leang C, Ueki T, Nevin KP, Lovley DR (2013) A genetic system for Clostridium ljungdahlii: a chassis for autotrophic production of biocommodities and a model homoacetogen. Appl Environ Microbiol 79:1102–1109PubMedPubMedCentralGoogle Scholar
  50. Levar C, Rollefson J, Bond D (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, pp 29–48Google Scholar
  51. Li J, Romine MF, Ward MJ (2007) Identification and analysis of a highly conserved chemotaxis gene cluster in Shewanella species. FEMS Microbiol Lett 273:180–186PubMedGoogle Scholar
  52. Liu J, Qiao Y, Lu ZS, Song H, Li CM (2012) Enhance electron transfer and performance of microbial fuel cells by perforating the cell membrane. Electrochem Commun 15:50–53Google Scholar
  53. Liu W, Lin J, Pang X, Cui S, Mi S, Lin J (2011) Overexpression of rusticyanin in Acidithiobacillus ferrooxidans ATCC19859 increased Fe(II) oxidation activity. Curr Microbiol 62:320–324PubMedGoogle Scholar
  54. Liu W, Lin J, Pang X, Mi S, Cui S, Lin J (2013) Increases of ferrous iron oxidation activity and arsenic stressed cell growth by overexpression of Cyc2 in Acidithiobacillus ferrooxidans ATCC19859. Biotechnol Appl Biochem 60:623–628PubMedGoogle Scholar
  55. Liu Z, Borne F, Ratouchniak J, Bonnefoy V (2001) Genetic transfer of IncP, IncQ and IncW plasmids to four Thiobacillus ferrooxidans strains by conjugation. Hydrometallurgy 59:339–345Google Scholar
  56. Liu Z, Guiliani N, Appia-Ayme C, Borne F, Ratouchniak J, Bonnefoy V (2000) Construction and characterization of arecA mutant of Thiobacillus ferrooxidans by marker exchange mutagenesis. J Bacteriol 182:2269–2276PubMedPubMedCentralGoogle Scholar
  57. Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381PubMedGoogle Scholar
  58. Logan BE (2010) Scaling up microbial fuel cells and other bioelectrochemical systems. Appl Microbiol Biotechnol 85:1665–1671PubMedGoogle Scholar
  59. Lohner ST, Deutzmann JS, Logan BE, Leigh J, Spormann AM (2014) Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis. The ISME journal 8:1673–1681PubMedGoogle Scholar
  60. Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJ, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445–448Google Scholar
  61. Maier TM, Myers CR (2004) The outer membrane protein Omp35 affects the reduction of Fe (III), nitrate, and fumarate by Shewanella oneidensis MR-1. BMC Microbiol 4:23PubMedPubMedCentralGoogle Scholar
  62. Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim B-C, Inoue K, Mester T, Covalla SF, Johnson JP (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6:573–579PubMedGoogle Scholar
  63. Malvankar NS, Tuominen MT, Lovley DR (2012) Comment on “On electrical conductivity of microbial nanowires and biofilms” by SM Strycharz-Glaven, RM Snider, A. Guiseppi-Elie and LM Tender, Energy Environ. Sci. Energy Environ Sci 5:6247–6249Google Scholar
  64. Marshall CW, Ross DE, Fichot EB, Norman RS, May HD (2013) Long-term operation of microbial electrosynthesis systems improves acetate production by autotrophic microbiomes. Environ Sci Technol 47:6023–6029PubMedGoogle Scholar
  65. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105:3968–3973PubMedPubMedCentralGoogle Scholar
  66. Matsumoto N, Nakasono S, Ohmura N, Saiki H (1999) Extension of logarithmic growth of Thiobacillus ferrooxidans by potential controlled electrochemical reduction of Fe(III). Biotechnol Bioeng 64:716–721PubMedGoogle Scholar
  67. Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, Thomashow LS (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183:6454–6465PubMedPubMedCentralGoogle Scholar
  68. McLean JS, Pinchuk GE, Geydebrekht OV, Bilskis CL, Zakrajsek BA, Hill EA, Saffarini D, Romine MF, Gorby YA, Fredrickson JK (2008) Oxygen dependent autoaggregation in Shewanella oneidensis MR1. Environ Microbiol 10:1861–1876PubMedGoogle Scholar
  69. Meshulam-Simon G, Behrens S, Choo AD, Spormann AM (2007) Hydrogen metabolism in Shewanella oneidensis MR-1. Appl Environ Microbiol 73:1153–1165PubMedPubMedCentralGoogle Scholar
  70. Methe B, Nelson KE, Eisen J, Paulsen I, Nelson W, Heidelberg J, Wu D, Wu M, Ward N, Beanan M (2003) Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302:1967–1969PubMedGoogle Scholar
  71. Meyer TE, Tsapin AI, Vandenberghe I, de Smet L, Frishman D, Nealson KH, Cusanovich MA, van Beeumen JJ (2004) Identification of 42 possible cytochrome C genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 8:57–77PubMedGoogle Scholar
  72. Möller B, Oßmer R, Howard BH, Gottschalk G, Hippe H (1984) Sporomusa, a new genus of gram-negative anaerobic bacteria including Sporomusa sphaeroides spec. nov. and Sporomusa ovata spec. nov. Arch Microbiol 139:388–396Google Scholar
  73. Myers CR, Myers JM (1997) Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J Bacteriol 179:1143–1152PubMedPubMedCentralGoogle Scholar
  74. Nagarajan H, Sahin M, Nogales J, Latif H, Lovley DR, Ebrahim A, Zengler K (2013) Characterizing acetogenic metabolism using a genome-scale metabolic reconstruction of Clostridium ljungdahlii. Microb Cell Factories 12:118Google Scholar
  75. Nakasono S, Matsumoto N, Saiki H (1997) Electrochemical cultivation of Thiobacillus ferrooxidans by potential control. Biotechnol Bioeng 43:61–66Google Scholar
  76. Nevin KP, Hensley SA, Franks AE, Summers ZM, Ou J, Woodard TL, Snoeyenbos-West OL, Lovley DR (2011) Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol 77:2882–2886PubMedPubMedCentralGoogle Scholar
  77. 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:e5628PubMedPubMedCentralGoogle Scholar
  78. Nevin KP, Lovley DR (2000) Lack of production of electron-shuttling compounds or solubilization of Fe(III) during reduction of insoluble Fe(III) oxide by Geobacter metallireducens. Appl Environ Microbiol 66:2248–2251PubMedPubMedCentralGoogle Scholar
  79. Nevin KP, Richter H, Covalla SF, Johnson JP, Woodard TL, Orloff AL, Jia H, Zhang M, Lovley DR (2008) Power output and columbic efficiencies from biofilms of Geobacter sulfurreducens comparable to mixed community microbial fuel cells. Environ Microbiol 10:2505–2514PubMedGoogle Scholar
  80. Nevin KP, Woodard TL, Franks AE, Summers ZM, Lovley DR (2010) Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. MBio 1(2):e00103–e00110PubMedPubMedCentralGoogle Scholar
  81. Ohmura N, Sasaki K, Matsumoto N, Saiki H (2002) Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans. J Bacteriol 184:2081–2087PubMedPubMedCentralGoogle Scholar
  82. Okamoto A, Hashimoto K, Nealson KH, Nakamura R (2013) Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proc Natl Acad Sci U S A 110:7856–7861PubMedPubMedCentralGoogle Scholar
  83. Peng J-B, Yan W-M, Bao X-Z (1994) Plasmid and transposon transfer to Thiobacillus ferrooxidans. J Bacteriol 176:2892–2897PubMedPubMedCentralGoogle Scholar
  84. Pierce E, Xie G, Barabote RD, Saunders E, Han CS, Detter JC, Richardson P, Brettin TS, Das A, Ljungdahl LG, Ragsdale SW (2008) The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ Microbiol 10:2550–2573PubMedPubMedCentralGoogle Scholar
  85. Poehlein A, Gottschalk G, Daniel R (2013) First insights into the genome of the Gram-negative, endospore-forming organism Sporomusa ovata strain H1 DSM 2662. Genome Announc 1(5):e00734–00713PubMedPubMedCentralGoogle Scholar
  86. Quatrini R, Appia-Ayme C, Denis Y, Ratouchniak J, Veloso F, Valdes J, Lefimil C, Silver S, Roberto F, Orellana O, Denizot F, Jedlicki E, Holmes D, Bonnefoy V (2006) Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling. Hydrometallurgy 83:263–272Google Scholar
  87. Rabaey K, Angenent L, Schröder U, Keller J (2010) Bioelectrochemical systems: from extracellular electrons transfer to biotechnological application. IWA Publishing, LondonGoogle Scholar
  88. Rabaey K, Boon N, Höfte M, Verstraete W (2005) Microbial phenazine production enhances electron transfer in biofuel cells. Environ Sci Technol 39:3401–3408PubMedGoogle Scholar
  89. Rabaey K, Boon N, Siciliano SD, Verhaege M, Verstraete W (2004) Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl Environ Microbiol 70:5373–5382PubMedPubMedCentralGoogle Scholar
  90. Rabaey K, Girguis P, Nielsen LK (2011) Metabolic and practical considerations on microbial electrosynthesis. Curr Opin Biotechnol 22:371–377PubMedGoogle Scholar
  91. Rao G, Mutharasan R (1987) Altered electron flow in continuous cultures of Clostridium acetobutylicum induced by viologen dyes. Appl Environ Microbiol 53:1232–1235PubMedPubMedCentralGoogle Scholar
  92. Rawlings DE (2001) The molecular genetics of Thiobacillus ferrooxidans and other mesophilic, acidophilic, chemolithotrophic, iron- or sulfur-oxidizing bacteria. Hydrometallurgy 59:187–201Google Scholar
  93. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101PubMedGoogle Scholar
  94. 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 72:7345–7348PubMedPubMedCentralGoogle Scholar
  95. Richter H, Nevin KP, Jia H, 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 2:506–516Google Scholar
  96. Richter LV, Sandler SJ, Weis RM (2012) Two isoforms of Geobacter sulfurreducens PilA have distinct roles in pilus biogenesis, cytochrome localization, extracellular electron transfer, and biofilm formation. J Bacteriol 194:2551–2563PubMedPubMedCentralGoogle Scholar
  97. 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 191:4207–4217PubMedPubMedCentralGoogle Scholar
  98. 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 193:1023–1033PubMedPubMedCentralGoogle Scholar
  99. Rosenbaum M, Aulenta F, Villano M, Angenent LT (2011) Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved? Bioresour Technol 102:324–333PubMedGoogle Scholar
  100. Rosenbaum M, Cotta MA, Angenent LT (2010) Aerated Shewanella oneidensis in continuously fed bioelectrochemical systems for power and hydrogen production. Biotechnol Bioeng 105:880–888PubMedGoogle Scholar
  101. Ross DE, Flynn JM, Baron DB, Gralnick JA, Bond DR (2011) Towards electrosynthesis in Shewanella: energetics of reversing the mtr pathway for reductive metabolism. PLoS One 6:e16649PubMedPubMedCentralGoogle Scholar
  102. Ross DE, Ruebush SS, Brantley SL, Hartshorne RS, Clarke TA, Richardson DJ, Tien M (2007) Characterization of protein-protein interactions involved in iron reduction by Shewanella oneidensis MR-1. Appl Environ Microbiol 73:5797–5808PubMedPubMedCentralGoogle Scholar
  103. Saville RM, Dieckmann N, Spormann AM (2010) Spatiotemporal activity of the mshA gene system in Shewanella oneidensis MR-1 biofilms. FEMS Microbiol Lett 308:76–83PubMedGoogle Scholar
  104. Saville RM, Rakshe S, Haagensen JA, Shukla S, Spormann AM (2011) Energy-dependent stability of Shewanella oneidensis MR-1 biofilms. J Bacteriol 193:3257–3264PubMedPubMedCentralGoogle Scholar
  105. Schiel-Bengelsdorf B, Dürre P (2012) Pathway engineering and synthetic biology using acetogens. FEBS Lett 586:2191–2198PubMedGoogle Scholar
  106. Schrott GD, Bonanni PS, Robuschi L, Esteve-Nuñez A, Busalmen JP (2011) Electrochemical insight into the mechanism of electron transport in biofilms of Geobacter sulfurreducens. Electrochim Acta 56:10791–10795Google Scholar
  107. Schwalb C, Chapman SK, Reid GA (2003) The tetraheme cytochrome CymA is required for anaerobic respiration with dimethyl sulfoxide and nitrite in Shewanella oneidensis. Biochemistry 42:9491–9497PubMedGoogle Scholar
  108. Strycharz SM, Glaven RH, Coppi MV, Gannon SM, Perpetua LA, Liu A, Nevin KP, Lovley DR (2011) Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry 80:142–150PubMedGoogle Scholar
  109. Strycharz SM, Woodard TL, Johnson JP, Nevin KP, Sanford RA, Loffler FE, Lovley DR (2008) Graphite electrode as a sole electron donor for reductive dechlorination of tetrachlorethene by Geobacter lovleyi. Appl Environ Microbiol 74:5943–5947PubMedPubMedCentralGoogle Scholar
  110. Strycharz-Glaven SM, Tender LM (2012) Reply to the ‘Comment on “On electrical conductivity of microbial nanowires and biofilms”’by NS Malvankar, MT Tuominen and DR Lovley, Energy Environ. Sci., 2012, 5, DOI: 10.1039/c2ee02613a, Energy Environ. Sci. 5:6250–6255Google Scholar
  111. 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 330:1413–1415PubMedGoogle Scholar
  112. Sundararajan A, Kurowski J, Yan T, Klingeman DM, Joachimiak MP, Zhou J, Naranjo B, Gralnick JA, Fields MW (2011) Shewanella oneidensis MR-1 sensory box protein involved in aerobic and anoxic growth. Appl Environ Microbiol 77:4647–4656PubMedPubMedCentralGoogle Scholar
  113. Tai SK, Wu G, Yuan S, Li KC (2010) Genome-wide expression links the electron transfer pathway of Shewanella oneidensis to chemotaxis. BMC Genomics 11:319PubMedPubMedCentralGoogle Scholar
  114. Tang YJ, Meadows AL, Keasling JD (2007) A kinetic model describing Shewanella oneidensis MR1 growth, substrate consumption, and product secretion. Biotechnol Bioeng 96:125–133PubMedGoogle Scholar
  115. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506PubMedPubMedCentralGoogle Scholar
  116. TerAvest MA, Rosenbaum MA, Kotloski NJ, Gralnick JA, Angenent LT (2013) Oxygen allows Shewanella oneidensis MR1 to overcome mediator washout in a continuously fed bioelectrochemical system. Biotechnol Bioeng 111(4):692–699Google Scholar
  117. Thormann KM, Saville RM, Shukla S, Pelletier DA, Spormann AM (2004) Initial phases of biofilm formation in Shewanella oneidensis MR-1. J Bacteriol 186:8096–8104PubMedPubMedCentralGoogle Scholar
  118. Thormann KM, Saville RM, Shukla S, Spormann AM (2005) Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J Bacteriol 187:1014–1021PubMedPubMedCentralGoogle Scholar
  119. Tremblay P-L, Zhang T, Dar SA, Leang C, Lovley DR (2013) The Rnf complex of Clostridium ljungdahlii is a proton-translocating ferredoxin:NAD + oxidoreductase essential for autotrophic growth. MBio 4(1):e00406–e00412PubMedCentralGoogle Scholar
  120. Tremblay PL, Aklujkar M, Leang C, Nevin KP, Lovley D (2012) A genetic system for Geobacter metallireducens: role of the flagellin and pilin in the reduction of Fe(III) oxide. Environ Microbiol Rep 4:82–88PubMedGoogle Scholar
  121. Valdés J, Pedroso I, Quatrini R, Holmes DS (2008) Comparative genome analysis of Acidithiobacillus ferrooxidans A thiooxidans and A caldus: insights into their metabolism and ecophysiology. Hydrometallurgy 94:180–184Google Scholar
  122. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS (2002) Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res 30:3141–3151PubMedPubMedCentralGoogle Scholar
  123. Wang H, Liu X, Liu S, Yu Y, Lin J, Lin J, Pang X, Zhao J (2012) Development of a markerless gene replacement system for Acidithiobacillus ferrooxidans and construction of a pfkB mutant. Appl Environ Microbiol 78:1826–1835PubMedPubMedCentralGoogle Scholar
  124. Wang VB, Kirchhofer ND, Chen X, Tan MYL, Sivakumar K, Cao B, Zhang Q, Kjelleberg S, Bazan GC, Loo SCJ (2014) Comparison of flavins and a conjugated oligoelectrolyte in stimulating extracellular electron transport from Shewanella oneidensis MR-1. Electrochem Commun 41:55–58Google Scholar
  125. Watnick P, Kolter R (2000) Biofilm, city of microbes. J Bacteriol 182:2675–2679PubMedPubMedCentralGoogle Scholar
  126. Yarzábal A, Appia-Ayme C, Ratouchniak J, Bonnefoy V (2004) Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology 150:2113–2123PubMedGoogle Scholar
  127. Yin J, Sun L, Dong Y, Chi X, Zhu W, S-h Q, Gao H (2013) Expression of blaA underlies unexpected ampicillin-induced cell lysis of Shewanella oneidensis. PLoS One 8:e60460PubMedPubMedCentralGoogle Scholar
  128. Yong YC, Yu YY, Yang Y, Liu J, Wang JY, Song H (2013) Enhancement of extracellular electron transfer and bioelectricity output by synthetic porin. Biotechnol Bioeng 110:408–416PubMedGoogle Scholar
  129. Yu Y-Y, H-l C, Yong Y-C, Kim D-H, Song H (2011) Conductive artificial biofilm dramatically enhances bioelectricity production in Shewanella-inoculated microbial fuel cells. Chem Commun 47:12825–12827Google Scholar
  130. Yu Y, Liu X, Wang H, Li X, Lin J (2014) Construction and characterization of tetH overexpression and knockout strains of Acidithiobacillus ferrooxidans. J Bacteriol 196(12):2255–2264PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Anne Sydow
    • 1
  • Thomas Krieg
    • 1
  • Florian Mayer
    • 1
  • Jens Schrader
    • 1
  • Dirk Holtmann
    • 1
  1. 1.Biochemical EngineeringDECHEMA-ForschungsinstitutFrankfurtGermany

Personalised recommendations