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Bioanalytical Reviews

, Volume 4, Issue 2–4, pp 159–192 | Cite as

Electron transfer mechanisms between microorganisms and electrodes in bioelectrochemical systems

  • Sunil A. PatilEmail author
  • Cecilia Hägerhäll
  • Lo Gorton
Article

Abstract

Microbes have been shown to naturally form veritable electric grids in which different species acting as electron donors and others acting as electron acceptors cooperate. The uptake of electrons from cells adjacent to them is a mechanism used by microorganisms to gain energy for cell growth and maintenance. The external discharge of electrons in lieu of a terminal electron acceptor, and the reduction of external substrates to uphold certain metabolic processes, also plays a significant role in a variety of microbial environments. These vital microbial respiration events, viz. extracellular electron transfer to and from microorganisms, have attracted widespread attention in recent decades and have led to the development of fascinating research concerning microbial electrochemical sensors and bioelectrochemical systems for environmental and bioproduction applications involving different fuels and chemicals. In such systems, microorganisms use mainly either (1) indirect routes involving use of small redox-active organic molecules referred to as redox mediators, secreted by cells or added exogenously, (2) primary metabolites or other intermediates, or (3) direct modes involving physical contact in which naturally occurring outer-membrane c-type cytochromes shuttle electrons for the reduction or oxidation of electrodes. Electron transfer mechanisms play a role in maximizing the performance of microbe–electrode interaction-based systems and help very much in providing an understanding of how such systems operate. This review summarizes the mechanisms of electron transfer between bacteria and electrodes, at both the anode and the cathode, in bioelectrochemical systems. The use over the years of various electrochemical approaches and techniques, cyclic voltammetry in particular, for obtaining a better understanding of the microbial electrocatalysis and the electron transfer mechanisms involved is also described and exemplified.

Keywords

Microbial extracellular electron transfer Microbe–electrode interactions Bioelectrochemical systems c-type cytochromes Redox mediators Nanowires Cyclic voltammetry 

Abbreviations

BESs

Bioelectrochemical systems

CA

Chronoamperometry

CV

Cyclic voltammetry

DET

Direct electron transfer

ET

Electron transfer

EET

Extracellular electron transfer

EABs

Electroactive biofilms

EIS

Electrochemical impedance spectroscopy

ITO

Tin-doped indium oxide

MFCs

Microbial fuel cells

MET

Mediated electron transfer

ORR

Oxygen reduction reaction

OMCs

Outer-membrane cytochromes

PQQ

Pyrroloquinoline quinone

SCE

Standard calomel electrode

ST

Substrate turnover

SNT

Substrate non-turnover

SHE

Standard hydrogen electrode

SEIRAS

Surface-enhanced infrared absorption spectroscopy

SERRS

Surface-enhanced resonance Raman spectroscopy

UV–Vis

Ultraviolet–Visible

Notes

Acknowledgments

The authors gratefully acknowledge the financial support provided by the Research Executive Agency (REA) of the European Union under Grant Agreement number PITN-GA-2010-264772 (ITN CHEBANA), the Swedish Research Council (2010-5031), and the nmC@LU.

References

  1. 1.
    Hernandez ME, Newman DK (2001) Extracellular electron transfer. Cell Mol Life Sci 58:1562–1571CrossRefGoogle Scholar
  2. 2.
    Heijnen JJ (1999) Bioenergetics of microbial growth. In: Flickinger MC, Drew SW (eds) Encyclopedia of bioprocess technology: fermentation, biocatalysis, bioseparation. Wiley, New York, pp 267–291Google Scholar
  3. 3.
    Rabaey K, Angenent L, Schröder U, Keller J (eds) (2010) Bioelectrochemical systems: from extracellular electron transfer to biotechnological application. IWA, LondonGoogle Scholar
  4. 4.
    Logan BE, Hamelers B, Rozendal R, Schröder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40:5181–5192CrossRefGoogle Scholar
  5. 5.
    Kato S, Hashimoto K, Watanabe K (2012) Microbial interspecies electron transfer via electric currents through conductive minerals. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1117592109
  6. 6.
    Lovley DR, Phillips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480Google Scholar
  7. 7.
    Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240:1319–1321CrossRefGoogle Scholar
  8. 8.
    Bentley A, Atkinson A, Jezek J, Rawson DM (2001) Whole cell biosensors—electrochemical and optical approaches to ecotoxicity testing. Toxicol in Vitro 15:469–475CrossRefGoogle Scholar
  9. 9.
    Pasco N, Weld R, Hay J, Gooneratne R (2011) Development and applications of whole cell biosensors for ecotoxicity testing. Anal Bioanal Chem 400:931–945CrossRefGoogle Scholar
  10. 10.
    Shimomura-Shimizu M, Karube I (2010) Applications of microbial cell sensors. In: Belkin S, Gu MB (eds) Whole cell sensing system II, vol 118. Springer, Berlin, pp 1–30CrossRefGoogle Scholar
  11. 11.
    Nakamura H, Shimomura-Shimizu M, Karube I (2008) Development of microbial sensors and their application. In: Renneberg R, Lisdat F (eds) Biosensing for the 21st century, vol 109. Springer, Berlin, pp 351–394CrossRefGoogle Scholar
  12. 12.
    Ding L, Du D, Zhang X, Ju H (2008) Trends in cell-based electrochemical biosensors. Curr Med Chem 15:3160–3170CrossRefGoogle Scholar
  13. 13.
    Su L, Jia W, Hou C, Lei Y (2011) Microbial biosensors: a review. Biosens Bioelectron 26:1788–1799CrossRefGoogle Scholar
  14. 14.
    Arends JBA, Verstraete W (2012) 100 years of microbial electricity production: three concepts for the future. Microb Biotechnol 5:333–346CrossRefGoogle Scholar
  15. 15.
    Schröder U (2011) Discover the possibilities: microbial bioelectrochemical systems and the revival of a 100-year-old discovery. J Solid State Electr 15:1481–1486CrossRefGoogle Scholar
  16. 16.
    Potter MC (1912) Electrical effects accompanying the decomposition of organic compounds. Proc Roy Soc London (B) 84:260–276CrossRefGoogle Scholar
  17. 17.
    Cohen B (1931) The bacterial culture as an electrical half-cell. J Bacteriol 21:18–19Google Scholar
  18. 18.
    Lewis K (1966) Biochemical fuel cells. Bacteriol Rev 30:101–113Google Scholar
  19. 19.
    Canfield JH, Goldner BH, Lutwack R (1963) Utilization of human wastes as electrochemical fuels. In: NASA Technical Report, Magna Corporation, Anaheim CA. p 63Google Scholar
  20. 20.
    Davis JB, Yarbrough HF (1962) Preliminary experiments on a microbial fuel cell. Science 137:615–616CrossRefGoogle Scholar
  21. 21.
    Ardeleanu I, Mǎrgineanu D-G, Vais H (1983) Electrochemical conversion in biofuel cells using Clostridium butyricum or Staphylococcus aureus Oxford. Bioelectrochem Bioenerg 11:273–277CrossRefGoogle Scholar
  22. 22.
    Karube I, Matsunga T, Tsuru S, Suzuki S (1977) Biochemical fuel cell utilizing immobilized cells of Clostridium butyricum. Biotechnol Bioeng 21:1727–1733CrossRefGoogle Scholar
  23. 23.
    Bennetto HP, Stirling JL, Tanaka K, Vega CA (1983) Anodic reactions in microbial fuel cells. Biotechnol Bioeng 25:559–568CrossRefGoogle Scholar
  24. 24.
    Akiba T, Bennetto HP, Stirling JL, Tanaka K (1987) Electricity production from alkalophilic organisms. Biotechnol Lett 9:611–616CrossRefGoogle Scholar
  25. 25.
    Tanaka K, Tamamushi R, Ogawa T (1985) Bioelectrochemical fuel-cells operated by the cyanobacterium, Anabaena variabilis. J Chem Technol Biot 35:191–197CrossRefGoogle Scholar
  26. 26.
    Allen RM, Bennetto HP (1993) Microbial fuel cells: electricity production from carbohydrates. Appl Biochem Biotech 39(40):27–40CrossRefGoogle Scholar
  27. 27.
    Zhang X-C, Halme A (1985) Modelling of a microbial fuel cell process. Biotechnol Lett 17:809–814CrossRefGoogle Scholar
  28. 28.
    Kim BH, Ikeda T, Park HS, Kim HJ, Hyun MS, Kano K, Takagi K, Tatsumi H (1999) Electrochemical activity of an Fe(III)-reducing bacterium, Shewanella putrefaciens IR-1, in the presence of alternative electron acceptors. Biotechnol Tech 13:475–478CrossRefGoogle Scholar
  29. 29.
    Yang Y, Sun G, Xu M (2011) Microbial fuel cells come of age. J Chem Technol Biot 86:625–632CrossRefGoogle Scholar
  30. 30.
    Oh ST, Kim JR, Premier GC, Lee TH, Kim C, Sloan WT (2011) Sustainable wastewater treatment: how might microbial fuel cells contribute. Biotechnol Adv 28:871–881CrossRefGoogle Scholar
  31. 31.
    Logan B (2010) Scaling up microbial fuel cells and other bioelectrochemical systems. Appl Microbiol Biot 85:1665–1671CrossRefGoogle Scholar
  32. 32.
    Logan BE (2008) Microbial fuel cells. Wiley, New YorkGoogle Scholar
  33. 33.
    Thrash JC, Coates JD (2008) Review: direct and indirect electrical stimulation of microbial metabolism. Environ Sci Technol 42:3921–3931CrossRefGoogle Scholar
  34. 34.
    Park DH, Zeikus JG (1999) Utilization of electrically reduced neutral red by Actinobacillus succinogenes: physiological function of neutral red in membrane-driven fumarate reduction and energy conservation. J Bacteriol 181:2403–2410Google Scholar
  35. 35.
    Park DH, Laivenieks M, Guettler MV, Jain MK, Zeikus JG (1999) Microbial utilization of electrically reduced neutral red as the sole electron donor for growth and metabolite production. Appl Environ Microbiol 65:2912–2917Google Scholar
  36. 36.
    Ro D-K, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MCY, Withers ST, Shiba Y, Sarpong R, Keasling JD (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:940–943CrossRefGoogle Scholar
  37. 37.
    ter Heijne A, Hamelers HVM, de Wilde V, Rozendal RA, Buisman CJN (2006) A bipolar membrane combined with ferric iron reduction as an efficient cathode system in microbial fuel cells. Environ Sci Technol 40:5200–5205CrossRefGoogle Scholar
  38. 38.
    Rhoads A, Beyenal H, Lewandowski Z (2005) Microbial fuel cell using anaerobic respiration as an anodic reaction and biomineralized manganese as a cathodic reactant. Environ Sci Technol 39:4666–4671CrossRefGoogle Scholar
  39. 39.
    He Z, Angenent LT (2006) Application of bacterial biocathodes in microbial fuel cells. Electroanal 18:2009–2015CrossRefGoogle Scholar
  40. 40.
    Rosenbaum M, Aulenta F, Villano M, Angenent LT (2011) Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved? Bioresource Technol 102:324–333CrossRefGoogle Scholar
  41. 41.
    Huang L, Regan JM, Quan X (2011) Electron transfer mechanisms, new applications, and performance of biocathode microbial fuel cells. Bioresource Technol 102:316–323CrossRefGoogle Scholar
  42. 42.
    Erable B, Féron D, Bergel A (2012) Microbial catalysis of the oxygen reduction reaction for microbial fuel cells: a review. ChemSusChem 5:975–987CrossRefGoogle Scholar
  43. 43.
    ter Heijne A, Strik DPBTB, Hamelers HVM, Buisman CJN (2010) Cathode potential and mass transfer determine performance of oxygen reducing biocathodes in microbial fuel cells. Environ Sci Technol 44:7151–7156CrossRefGoogle Scholar
  44. 44.
    Rabaey K, Read ST, Clauwaert P, Freguia S, Bond PL, Blackall LL, Keller J (2008) Cathodic oxygen reduction catalyzed by bacteria in microbial fuel cells. ISME J 2:519–527CrossRefGoogle Scholar
  45. 45.
    Chung K, Fujiki I, Okabe S (2011) Effect of formation of biofilms and chemical scale on the cathode electrode on the performance of a continuous two-chamber microbial fuel cell. Bioresource Technol 102:355–360CrossRefGoogle Scholar
  46. 46.
    Cournet A, Bergé M, Roques C, Bergel A, Délia M-L (2010) Electrochemical reduction of oxygen catalyzed by Pseudomonas aeruginosa. Electrochim Acta 55:4902–4908CrossRefGoogle Scholar
  47. 47.
    Clauwaert P, van der Ha D, Boon N, Verbeken K, Verhaege M, Rabaey K, Verstraete W (2007) Open air biocathode enables effective electricity generation with microbial fuel cells. Environ Sci Technol 41:7564–7569CrossRefGoogle Scholar
  48. 48.
    Prasad D, Sivaram TK, Berchmans S, Yegnaraman V (2006) Microbial fuel cell constructed with a micro-organism isolated from sugar industry effluent. J Power Sources 160:991–996CrossRefGoogle Scholar
  49. 49.
    Bergel A, Féron D, Mollica A (2005) Catalysis of oxygen reduction in PEM fuel cell by seawater biofilm. Electrochem Commun 7:900–904CrossRefGoogle Scholar
  50. 50.
    Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6:596–604CrossRefGoogle Scholar
  51. 51.
    Lefebvre O, Al-Mamun A, Ng HY (2008) A microbial fuel cell equipped with a biocathode for organic removal and denitrification. Water Sci Technol 58:881–885CrossRefGoogle Scholar
  52. 52.
    Clauwaert P, Rabaey K, Aelterman P, De Schamphelaire L, Pham TH, Boeckx P, Boon N, Verstraete W (2007) Biological denitrification in microbial fuel cells. Environ Sci Technol 41:3354–3360CrossRefGoogle Scholar
  53. 53.
    Rozendal RA, Hamelers HVM, Euverink GJW, Metz SJ, Buisman CJN (2006) Principle and perspectives of hydrogen production through biocatalyzed electrolysis. Int J Hydrogen Energ 31:1632–1640CrossRefGoogle Scholar
  54. 54.
    Cheng S, Logan BE (2007) Sustainable and efficient biohydrogen production via electrohydrogenesis. Proc Natl Acad Sci USA 104:18871–18873CrossRefGoogle Scholar
  55. 55.
    Rinaldi A, Mecheri B, Garavaglia V, Licoccia S, Di Nardo P, Traversa E (2008) Engineering materials and biology to boost performance of microbial fuel cells: a critical review. Energ Environ Sci 1:417–429CrossRefGoogle Scholar
  56. 56.
    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:e00103–e00110CrossRefGoogle Scholar
  57. 57.
    Rabaey K, Rozendal RA (2010) Microbial electrosynthesis—revisiting the electrical route for microbial production. Nat Rev Microbiol 8:706–716CrossRefGoogle Scholar
  58. 58.
    Lovley DR, Nevin KP (2011) A shift in the current: new applications and concepts for microbe-electrode electron exchange. Curr Opin Biotech 22:441–448CrossRefGoogle Scholar
  59. 59.
    Virdis B, Read ST, Rabaey K, Rozendal RA, Yuan Z, Keller J (2011) Biofilm stratification during simultaneous nitrification and denitrification (SND) at a biocathode. Bioresource Technol 102:334–341CrossRefGoogle Scholar
  60. 60.
    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 Microb 77:2882–2886CrossRefGoogle Scholar
  61. 61.
    Wrighton KC, Virdis B, Clauwaert P, Read ST, Daly RA, Boon N, Piceno Y, Andersen GL, Coates JD, Rabaey K (2010) Bacterial community structure corresponds to performance during cathodic nitrate reduction. ISME J 4:1443–1455CrossRefGoogle Scholar
  62. 62.
    Strycharz SM, Gannon SM, Boles AR, Franks AE, Nevin KP, Lovley DR (2010) Reductive dechlorination of 2-chlorophenol by Anaeromyxobacter dehalogenans with an electrode serving as the electron donor. Environ Microbiol Reports 2:289–294CrossRefGoogle Scholar
  63. 63.
    Rozendal RA, Leone E, Keller J, Rabaey K (2009) Efficient hydrogen peroxide generation from organic matter in a bioelectrochemical system. Electrochem Commun 11:1752–1755CrossRefGoogle Scholar
  64. 64.
    Fu L, You S-J, Yang F-L, Gao M-M, Fang X-H, Zhang G-Q (2010) Synthesis of hydrogen peroxide in microbial fuel cell. J Chem Technol Biot 85:715–719CrossRefGoogle Scholar
  65. 65.
    Butler CS, Clauwaert P, Green SJ, Verstraete W, Nerenberg R (2010) Bioelectrochemical perchlorate reduction in a microbial fuel cell. Environ Sci Technol 44:4685–4691CrossRefGoogle Scholar
  66. 66.
    Tandukar M, Huber SJ, Onodera T, Pavlostathis SG (2009) Biological chromium(VI) reduction in the cathode of a microbial fuel cell. Environ Sci Technol 43:8159–8165CrossRefGoogle Scholar
  67. 67.
    Mu Y, Rozendal RA, Rabaey K, Keller J (2009) Nitrobenzene removal in bioelectrochemical systems. Environ Sci Technol 43:8690–8695CrossRefGoogle Scholar
  68. 68.
    Zhang T, Gannon SM, Nevin KP, Franks AE, Lovley DR (2010) Stimulating the anaerobic degradation of aromatic hydrocarbons in contaminated sediments by providing an electrode as the electron acceptor. Environ Microbiol 12:1011–1020CrossRefGoogle Scholar
  69. 69.
    Mu Y, Rabaey K, Rozendal RA, Yuan Z, Keller J (2009) Decolorization of azo dyes in bioelectrochemical systems. Environ Sci Technol 43:5137–5143CrossRefGoogle Scholar
  70. 70.
    Jacobson KS, Drew DM, He Z (2011) Efficient salt removal in a continuously operated upflow microbial desalination cell with an air cathode. Bioresource Technol 102:376–380CrossRefGoogle Scholar
  71. 71.
    Cao X, Huang X, Liang P, Xiao K, Zhou Y, Zhang X, Logan BE (2009) A new method for water desalination using microbial desalination cells. Environ Sci Technol 43:7148–7152CrossRefGoogle Scholar
  72. 72.
    Kim Y, Logan BE (2012) Microbial desalination cells for energy production and desalination. Desalination. http://dx.doi.org/10.1016/j.desal.2012.07.022
  73. 73.
    Mehanna M, Basséguy R, Délia M-L, Bergel A (2010) Geobacter sulfurreducens can protect 304 L stainless steel against pitting in conditions of low electron acceptor concentrations. Electrochem Commun 12:724–728CrossRefGoogle Scholar
  74. 74.
    ter Heijne A, Liu F, Weijden RVD, Weijma J, Buisman CJN, Hamelers HVM (2010) Copper recovery combined with electricity production in a microbial fuel cell. Environ Sci Technol 44:4376–4381CrossRefGoogle Scholar
  75. 75.
    Villano M, De Bonis L, Rossetti S, Aulenta F, Majone M (2011) Bioelectrochemical hydrogen production with hydrogenophilic dechlorinating bacteria as electrocatalytic agents. Bioresource Technol 102:3193–3199CrossRefGoogle Scholar
  76. 76.
    Jeremiasse AW, Hamelers HVM, Buisman CJN (2010) Microbial electrolysis cell with a microbial biocathode. Bioelectrochemistry 78:39–43CrossRefGoogle Scholar
  77. 77.
    Geelhoed JS, Stams AJM (2010) Electricity-assisted biological hydrogen production from acetate by Geobacter sulfurreducens. Environ Sci Technol 45:815–820CrossRefGoogle Scholar
  78. 78.
    Aulenta F, Catapano L, Snip L, Villano M, Majone M (2012) Linking bacterial metabolism to graphite cathodes: electrochemical insights into the H2-producing capability of Desulfovibrio sp. ChemSusChem 5:1080–1085CrossRefGoogle Scholar
  79. 79.
    Modin O, Fukushi K (2012) Development and testing of bioelectrochemical reactors converting wastewater organics into hydrogen peroxide. Water Sci Technol 66:831–836CrossRefGoogle Scholar
  80. 80.
    van Eerten-Jansen MCAA, ter Heijne A, Buisman CJN, Hamelers HVM (2012) Microbial electrolysis cells for production of methane from CO2: long-term performance and perspectives. Int J Energ Res 36:809–819CrossRefGoogle Scholar
  81. 81.
    Villano M, Aulenta F, Ciucci C, Ferri T, Giuliano A, Majone M (2010) Bioelectrochemical reduction of CO2 to CH4 via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture. Bioresource Technol 101:3085–3090CrossRefGoogle Scholar
  82. 82.
    Cheng S, Xing D, Call DF, Logan BE (2009) Direct biological conversion of electrical current into methane by electromethanogenesis. Environ Sci Technol 43:3953–3958CrossRefGoogle Scholar
  83. 83.
    Luo H, Jenkins PE, Ren Z (2010) Concurrent desalination and hydrogen generation using microbial electrolysis and desalination cells. Environ Sci Technol 45:340–344CrossRefGoogle Scholar
  84. 84.
    Di Lorenzo M, Curtis TP, Head IM, Scott K (2009) A single-chamber microbial fuel cell as a biosensor for wastewaters. Water Res 43:3145–3154CrossRefGoogle Scholar
  85. 85.
    Stein NE, Keesman KJ, Hamelers HVM, van Straten G (2011) Kinetic models for detection of toxicity in a microbial fuel cell based biosensor. Biosens Bioelectron 26:3115–3120CrossRefGoogle Scholar
  86. 86.
    Peixoto L, Min B, Martins G, Brito AG, Kroff P, Parpot P, Angelidaki I, Nogueira R (2011) In situ microbial fuel cell-based biosensor for organic carbon. Bioelectrochemistry 81:99–103CrossRefGoogle Scholar
  87. 87.
    Dávila D, Esquivel JP, Sabaté N, Mas J (2011) Silicon-based microfabricated microbial fuel cell toxicity sensor. Biosens Bioelectron 26:2426–2430CrossRefGoogle Scholar
  88. 88.
    Di Lorenzo M, Curtis TP, Head IM, Velasquez-Orta SB, Scott K (2009) A single chamber packed bed microbial fuel cell biosensor for measuring organic content of wastewater. Water Sci Technol 60:2879–2887CrossRefGoogle Scholar
  89. 89.
    Tront JM, Fortner JD, Plötze M, Hughes JB, Puzrin AM (2008) Microbial fuel cell biosensor for in situ assessment of microbial activity. Biosens Bioelectron 24:586–590CrossRefGoogle Scholar
  90. 90.
    Kumlanghan A, Liu J, Thavarungkul P, Kanatharana P, Mattiasson B (2007) Microbial fuel cell-based biosensor for fast analysis of biodegradable organic matter. Biosens Bioelectron 22:2939–2944CrossRefGoogle Scholar
  91. 91.
    Kim BH, Chang IS, Gil GC, Park HS, Kim HJ (2003) Novel BOD (biological oxygen demand) sensor using mediator-less microbial fuel cell. Biotechnol Lett 25:541–545CrossRefGoogle Scholar
  92. 92.
    Patil S, Harnisch F, Schröder U (2010) Toxicity response of electroactive microbial biofilms—a decisive feature for potential biosensor and power source applications. Chemphyschem 11:2834–2837CrossRefGoogle Scholar
  93. 93.
    Harnisch F, Schröder U (2010) From MFC to MXC: chemical and biological cathodes and their potential for microbial bioelectrochemical systems. Chem Soc Rev 39:4433–4448CrossRefGoogle Scholar
  94. 94.
    Rabaey K, Verstraete W (2005) Microbial fuel cells: novel biotechnology for energy generation. Trends Biotechnol 23:291–298CrossRefGoogle Scholar
  95. 95.
    Hochella MF, Lower SK, Maurice PA, Penn RL, Sahai N, Sparks DL, Twining BS (2008) Nanominerals, mineral nanoparticles, and earth systems. Science 319:1631–1635CrossRefGoogle Scholar
  96. 96.
    Nealson K, Belz A, McKee B (2002) Breathing metals as a way of life: geobiology in action. A Van Leeuw 81:215–222CrossRefGoogle Scholar
  97. 97.
    Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55:259–287Google Scholar
  98. 98.
    Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764CrossRefGoogle Scholar
  99. 99.
    Nealson KH, Finkel SE (2011) Electron flow and biofilms. MRS Bull 36:380–384CrossRefGoogle Scholar
  100. 100.
    Lovley DR (1993) Dissimilatory metal reduction. Annu Rev Microbiol 47:263–290CrossRefGoogle Scholar
  101. 101.
    Nealson KH, Saffarini D (1994) Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu Rev Microbiol 48:311–343CrossRefGoogle Scholar
  102. 102.
    Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, Rodionov DA, Rodrigues JLM, Saffarini DA, Serres MH, Spormann AM, Zhulin IB, Tiedje JM (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6:592–603CrossRefGoogle Scholar
  103. 103.
    Lonergan DJ, Jenter HL, Coates JD, Phillips EJ, Schmidt TM, Lovley DR (1996) Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria. J Bacteriol 178:2402–2408Google Scholar
  104. 104.
    Lovley DR (1995) Microbial reduction of iron, manganese, and other metals. In: Donald LS (ed) Advances in agronomy, vol 54. Academic, New York, pp 175–231Google Scholar
  105. 105.
    Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru A-E Holmes DE, Franks AE, Orellana R, Risso C, Nevin KP (2011) Geobacter: the microbe electric’s physiology, ecology, and practical applications. Adv Microb Physiol 59:1–100CrossRefGoogle Scholar
  106. 106.
    Mahadevan R, Palsson BØ, 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 9:39–50CrossRefGoogle Scholar
  107. 107.
    Nealson K, Scott J (2006) Ecophysiology of the genus Shewanella. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 1133–1151CrossRefGoogle Scholar
  108. 108.
    Carmona-Martinez AA, Harnisch F, Kuhlicke U, Neu TR, Schröder U (2012) Electron transfer and biofilm formation of Shewanella putrefaciens as function of anode potential. Bioelectrochemistry. doi: 10.1016/j.bioelechem.2012.05.002
  109. 109.
    Yang Y, Xu M, Guo J, Sun G (2012) Bacterial extracellular electron transfer in bioelectrochemical systems. Process Biochem http://dx.doi.org/10.1016/j.procbio.2012.07.032
  110. 110.
    Yuan Y, Ahmed J, Zhou L, Zhao B, Kim S (2011) Carbon nanoparticles-assisted mediator-less microbial fuel cells using Proteus vulgaris. Biosens Bioelectron 27:106–112CrossRefGoogle Scholar
  111. 111.
    Kim N, Choi Y, Jung S, Kim S (2000) Effect of initial carbon sources on the performance of microbial fuel cells containing Proteus vulgaris. Biotechnol Bioeng 70:109–114CrossRefGoogle Scholar
  112. 112.
    Venkataraman A, Rosenbaum M, Arends JBA, Halitschke R, Angenent LT (2010) Quorum sensing regulates electric current generation of Pseudomonas aeruginosa PA14 in bioelectrochemical systems. Electrochem Commun 12:459–462CrossRefGoogle Scholar
  113. 113.
    Pham T, Boon N, Aelterman P, Clauwaert P, De Schamphelaire L, Vanhaecke L, De Maeyer K, Höfte M, Verstraete W, Rabaey K (2008) Metabolites produced by Pseudomonas sp. enable gram positive bacterium to achieve extracellular electron transfer. Appl Microbiol Biot 77:1119–1129CrossRefGoogle Scholar
  114. 114.
    Timur S, Haghighi B, Tkac J, Pazarlioglu N, Telefoncu A, Gorton L (2007) Electrical wiring of Pseudomonas putida and Pseudomonas fluorescens with osmium redox polymers. Bioelectrochemistry 71:38–45CrossRefGoogle Scholar
  115. 115.
    Weld RJ, Glithero N, Pasco N (2011) Escherichia coli knock-out mutants with altered electron transfer activity in the Micredox® assay and in microbial fuel cells. Int J Environ Anal Chem 91:138–149CrossRefGoogle Scholar
  116. 116.
    Veer Raghavulu S, Sarma PN, Venkata Mohan S (2011) Comparative bioelectrochemical analysis of Pseudomonas aeruginosa and Escherichia coli with anaerobic consortia as anodic biocatalyst for biofuel cell application. J Appl Microbiol 110:666–674CrossRefGoogle Scholar
  117. 117.
    Xia X, Cao X-X, Liang P, Huang X, Yang S-P, Zhao G-G (2010) Electricity generation from glucose by a Klebsiella sp. in microbial fuel cells. Appl Microbiol Biot 87(1):383–390CrossRefGoogle Scholar
  118. 118.
    Deng L, Li F, Zhou S, Huang D, Ni J (2010) A study of electron-shuttle mechanism in Klebsiella pneumoniae based-microbial fuel cells. Chinese Sci Bull 55:99–104CrossRefGoogle Scholar
  119. 119.
    Zhang L, Zhou S, Zhuang L, Li W, Zhang J, Lu N, Deng L (2008) Microbial fuel cell based on Klebsiella pneumoniae biofilm. Electrochem Commun 10:1641–1643CrossRefGoogle Scholar
  120. 120.
    Nimje VR, Chen C-Y, Chen C-C, Jean J-S, Reddy AS, Fan C-W, Pan K-Y, Liu H-T, Chen J-L (2009) Stable and high energy generation by a strain of Bacillus subtilis in a microbial fuel cell. J Power Sources 190(2):258–263CrossRefGoogle Scholar
  121. 121.
    Liu M, Yuan Y, Zhang L-X, Zhuang L, Zhou S-G, Ni J-R (2010) Bioelectricity generation by a Gram-positive Corynebacterium sp. strain MFC03 under alkaline condition in microbial fuel cells. Bioresource Technol 101:1807–1811CrossRefGoogle Scholar
  122. 122.
    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 54:4979–4984CrossRefGoogle Scholar
  123. 123.
    Coman V, Gustavsson T, Finkelsteinas A, von Wachenfeldt C, Hägerhäll C, Gorton L (2009) Electrical wiring of live, metabolically enhanced Bacillus subtilis cells with flexible osmium-redox polymers. J Am Chem Soc 131:16171–16176CrossRefGoogle Scholar
  124. 124.
    Schaetzle O, Barriere F, Baronian K (2008) Bacteria and yeasts as catalysts in microbial fuel cells: electron transfer from microorganisms to electrodes for green electricity. Energ Environ Sci 1:607–620CrossRefGoogle Scholar
  125. 125.
    Sharma V, Kundu PP (2010) Biocatalysts in microbial fuel cells. Enzyme Microb Tech 47(5):179–188CrossRefGoogle Scholar
  126. 126.
    Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381CrossRefGoogle Scholar
  127. 127.
    Rabaey K, Rodriguez J, Blackall LL, Keller J, Gross P, Batstone D, Verstraete W, Nealson KH (2007) Microbial ecology meets electrochemistry: electricity-driven and driving communities. ISME J 1:9–18CrossRefGoogle Scholar
  128. 128.
    Kiely PD, Regan JM, Logan BE (2011) The electric picnic: synergistic requirements for exoelectrogenic microbial communities. Curr Opin Biotech 22:378–385CrossRefGoogle Scholar
  129. 129.
    Wrighton KC, Agbo P, Warnecke F, Weber KA, Brodie EL, DeSantis TZ, Hugenholtz P, Andersen GL, Coates JD (2008) A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. ISME J 2:1146–1156CrossRefGoogle Scholar
  130. 130.
    Patil SA, Surakasi VP, Koul S, Ijmulwar S, Vivek A, Shouche YS, Kapadnis BP (2009) Electricity generation using chocolate industry wastewater and its treatment in activated sludge based microbial fuel cell and analysis of developed microbial community in the anode chamber. Bioresource Technol 100:5132–5139CrossRefGoogle Scholar
  131. 131.
    Jung S, Regan J (2007) Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors. Appl Microbiol Biot 77:393–402CrossRefGoogle Scholar
  132. 132.
    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. Bioresource Technol 100:3518–3525CrossRefGoogle Scholar
  133. 133.
    Raghavulu SV, Goud RK, Sarma PN, Mohan SV (2011) Saccharomyces cerevisiae as anodic biocatalyst for power generation in biofuel cell: Influence of redox condition and substrate load. Bioresource Technol 102:2751–2757CrossRefGoogle Scholar
  134. 134.
    Ducommun R, Favre M-F, Carrard D, Fischer F (2010) Outward electron transfer by Saccharomyces cerevisiae monitored with a bi-cathodic microbial fuel cell-type activity sensor. Yeast 27:139–148Google Scholar
  135. 135.
    Walker AL, Walker CW Jr (2006) Biological fuel cell and an application as a reserve power source. J Power Sources 160:123–129CrossRefGoogle Scholar
  136. 136.
    Haslett ND, Rawson FJ, Barriëre F, Kunze G, Pasco N, Gooneratne R, Baronian KHR (2011) Characterisation of yeast microbial fuel cell with the yeast Arxula adeninivorans as the biocatalyst. Biosens Bioelectron 26:3742–3747CrossRefGoogle Scholar
  137. 137.
    Shkil H, Schulte A, Guschin DA, Schuhmann W (2011) Electron transfer between genetically modified Hansenula polymorpha yeast cells and electrode surfaces via Os-complex modified redox polymers. Chemphyschem 12:806–813CrossRefGoogle Scholar
  138. 138.
    Prasad D, Arun S, Murugesan M, Padmanaban S, Satyanarayanan RS, Berchmans S, Yegnaraman V (2007) Direct electron transfer with yeast cells and construction of a mediatorless microbial fuel cell. Biosens Bioelectron 22:2604–2610CrossRefGoogle Scholar
  139. 139.
    Babanova S, Hubenova Y, Mitov M (2011) Influence of artificial mediators on yeast-based fuel cell performance. J Biosci Bioeng 112:379–387CrossRefGoogle Scholar
  140. 140.
    Richter H, Lanthier M, Nevin KP, Lovley DR (2007) Lack of electricity production by Pelobacter carbinolicus indicates that the capacity for Fe(III) oxide reduction does not necessarily confer electron transfer ability to fuel cell anodes. Appl Environ Microbiol 73:5347–5353CrossRefGoogle Scholar
  141. 141.
    Dumas C, Basseguy R, Bergel A (2008) Microbial electrocatalysis with Geobacter sulfurreducens biofilm on stainless steel cathodes. Electrochim Acta 53:2494–2500CrossRefGoogle Scholar
  142. 142.
    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:e16649CrossRefGoogle Scholar
  143. 143.
    Liu H, Matsuda S, Hashimoto K, Nakanishi S (2012) Flavins secreted by bacterial cells of Shewanella catalyze cathodic oxygen reduction. Chem Sus Chem 5:1054–1058Google Scholar
  144. 144.
    Hsu L, Masuda SA, Nealson KH, Pirbazari M (2012) Evaluation of microbial fuel cell Shewanella biocathodes for treatment of chromate contamination. RSC Adv 2:5844–5855CrossRefGoogle Scholar
  145. 145.
    Cournet A, Délia M-L, Bergel A, Roques C, Bergé M (2010) Electrochemical reduction of oxygen catalyzed by a wide range of bacteria including Gram-positive. Electrochem Commun 12:505–508CrossRefGoogle Scholar
  146. 146.
    Cheng KY, Ho G, Cord-Ruwisch R (2009) Anodophilic biofilm catalyzes cathodic oxygen reduction. Environ Sci Technol 44:518–525CrossRefGoogle Scholar
  147. 147.
    Erable B, Vandecandelaere I, Faimali M, Délia M-L, Etcheverry L, Vandamme P, Bergel A (2010) Marine aerobic biofilm as biocathode catalyst. Bioelectrochemistry 78:51–56CrossRefGoogle Scholar
  148. 148.
    Rozendal RA, Jeremiasse AW, Hamelers HVM, Buisman CJN (2007) Hydrogen production with a microbial biocathode. Environ Sci Technol 42:629–634CrossRefGoogle Scholar
  149. 149.
    Lovley DR (2011) Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ Microbiol Reports 3:27–35CrossRefGoogle Scholar
  150. 150.
    Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286CrossRefGoogle Scholar
  151. 151.
    Fredrickson JK, Zachara JM (2008) Electron transfer at the microbe–mineral interface: a grand challenge in biogeochemistry. Geobiology 6:245–253CrossRefGoogle Scholar
  152. 152.
    Shi L, Squier TC, Zachara JM, Fredrickson JK (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65:12–20CrossRefGoogle Scholar
  153. 153.
    Lovley DR (2011) Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energ Environ Sci 4:4896–4906CrossRefGoogle Scholar
  154. 154.
    Richardson DJ, Butt JN, Fredrickson JK, Zachara JM, Shi L, Edwards MJ, White G, Baiden N, Gates AJ, Marritt SJ, Clarke TA (2012) The ‘porin–cytochrome’ model for microbe-to-mineral electron transfer. Mol Microbiol 85:201–212CrossRefGoogle Scholar
  155. 155.
    Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS, Culley DE, Reed SB, Romine MF, Saffarini DA, Hill EA, Shi L, Elias DA, Kennedy DW, Pinchuk G, Watanabe K, Ishii S, Logan B, Nealson KH, Fredrickson JK (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci USA 103:11358–11363CrossRefGoogle Scholar
  156. 156.
    Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101CrossRefGoogle Scholar
  157. 157.
    Esteve-Núñez A, Sosnik J, Visconti P, Lovley DR (2008) Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens. Environ Microbiol 10:497–505CrossRefGoogle Scholar
  158. 158.
    Peng L, You S-J, Wang J-Y (2010) Electrode potential regulates cytochrome accumulation on Shewanella oneidensis cell surface and the consequence to bioelectrocatalytic current generation. Biosens Bioelectron 25:2530–2533CrossRefGoogle Scholar
  159. 159.
    Lovley DR (2008) Extracellular electron transfer: wires, capacitors, iron lungs, and more. Geobiology 6:225–231CrossRefGoogle Scholar
  160. 160.
    Qian X, Mester T, Morgado L, Arakawa T, Sharma ML, Inoue K, Joseph C, Salgueiro CA, Maroney MJ, Lovley DR (2011) Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens. BBA Bioenergetics 1807:404–412CrossRefGoogle Scholar
  161. 161.
    Tremblay P-L, Summers ZM, Glaven RH, Nevin KP, Zengler K, Barrett CL, Qiu Y, Palsson BO, Lovley DR (2011) A c-type cytochrome and a transcriptional regulator responsible for enhanced extracellular electron transfer in Geobacter sulfurreducens revealed by adaptive evolution. Environ Microbiol 13:13–23CrossRefGoogle Scholar
  162. 162.
    Shi L, Richardson DJ, Wang Z, Kerisit SN, Rosso KM, Zachara JM, Fredrickson JK (2009) The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ Microbiol Reports 1:220–227CrossRefGoogle Scholar
  163. 163.
    Richter K, Schicklberger M, Gescher J (2012) Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl Environ Microbiol 78:913–921CrossRefGoogle Scholar
  164. 164.
    Holmes DE, Mester T, O’Neil RA, Perpetua LA, Larrahondo MJ, Glaven R, Sharma ML, Ward JE, Nevin KP, Lovley DR (2008) 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 154:1422–1435CrossRefGoogle Scholar
  165. 165.
    Voordeckers JW, Kim B-C, Izallalen M, Lovley DR (2010) Role of Geobacter sulfurreducens outer surface c-type cytochromes in reduction of soil humic acid and anthraquinone-2,6-disulfonate. Appl Environ Microbiol 76:2371–2375CrossRefGoogle Scholar
  166. 166.
    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 USA 105:3968–3973CrossRefGoogle Scholar
  167. 167.
    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 74:615–623CrossRefGoogle Scholar
  168. 168.
    Lovley DR, Fraga JL, Blunt-Harris EL, Hayes LA, Phillips EJP, Coates JD (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydroch Hydrob 26:152–157CrossRefGoogle Scholar
  169. 169.
    Newman DK, Kolter R (2000) A role for excreted quinones in extracellular electron transfer. Nature 405:94–97CrossRefGoogle Scholar
  170. 170.
    Pierson L, Pierson E (2010) Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biot 86:1659–1670CrossRefGoogle Scholar
  171. 171.
    Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK (2005) Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Appl Environ Microbiol 71:4414–4426CrossRefGoogle Scholar
  172. 172.
    Jeans C, Singer SW, Chan CS, VerBerkmoes NC, Shah M, Hettich RL, Banfield JF, Thelen MP (2008) Cytochrome 572 is a conspicuous membrane protein with iron oxidation activity purified directly from a natural acidophilic microbial community. ISME J 2:542–550CrossRefGoogle Scholar
  173. 173.
    Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583CrossRefGoogle Scholar
  174. 174.
    Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G, Brugna M, Giudici-Orticoni M-T (2008) A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J Biol Chem 283:25803–25811CrossRefGoogle Scholar
  175. 175.
    Yarzábal A, Brasseur G, Ratouchniak J, Lund K, Lemesle-Meunier D, DeMoss JA, Bonnefoy V (2002) The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol 184:313–317CrossRefGoogle Scholar
  176. 176.
    Singer SW, Chan CS, Zemla A, VerBerkmoes NC, Hwang M, Hettich RL, Banfield JF, Thelen MP (2008) Characterization of cytochrome 579, an unusual cytochrome isolated from an iron-oxidizing microbial community. Appl Environ Microbiol 74:4454–4462CrossRefGoogle Scholar
  177. 177.
    Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555CrossRefGoogle Scholar
  178. 178.
    Okamoto A, Hashimoto K, Nakamura R (2012) Long-range electron conduction of Shewanella biofilms mediated by outer membrane c-type cytochromes. Bioelectrochemistry 85:61–65CrossRefGoogle Scholar
  179. 179.
    Busalmen JP, Esteve-Núñez A, Berná A, Feliu JM (2008) C-type cytochromes wire electricity-producing bacteria to electrodes. Angew Chem Int Edit 47:4874–4877CrossRefGoogle Scholar
  180. 180.
    El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G, Yang J, Lau WM, Nealson KH, Gorby YA (2010) Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci USA 107:18127–18131CrossRefGoogle Scholar
  181. 181.
    Rabaey K, Boon N, Höfte M, Verstraete W (2005) Microbial phenazine production enhances electron transfer in biofuel cells. Environ Sci Technol 39:3401–3408CrossRefGoogle Scholar
  182. 182.
    Park DH, Zeikus JG (2000) Electricity generation in microbial fuel cells using neutral red as an electronophore. Appl Environ Microbiol 66:1292–1297CrossRefGoogle Scholar
  183. 183.
    Tang X, Du Z, Li H (2010) Anodic electron shuttle mechanism based on 1-hydroxy-4-aminoanthraquinone in microbial fuel cells. Electrochem Commun 12:1140–1143CrossRefGoogle Scholar
  184. 184.
    Feng C, Ma L, Li F, Mai H, Lang X, Fan S (2010) A polypyrrole/anthraquinone-2,6-disulphonic disodium salt (PPy/AQDS)-modified anode to improve performance of microbial fuel cells. Biosens Bioelectron 25:1516–1520CrossRefGoogle Scholar
  185. 185.
    Rosenbaum M, Zhao F, Schröder U, Scholz F (2006) Interfacing electrocatalysis and biocatalysis with tungsten carbide: a high-performance, noble-metal-free microbial fuel cell. Angew Chem Int Edit 45:6658–6661CrossRefGoogle Scholar
  186. 186.
    Niessen J, Schröder U, Rosenbaum M, Scholz F (2004) Fluorinated polyanilines as superior materials for electrocatalytic anodes in bacterial fuel cells. Electrochem Commun 6:571–575CrossRefGoogle Scholar
  187. 187.
    Schröder U, Nießen J, Scholz F (2003) A generation of microbial fuel cells with current outputs boosted by more than one order of magnitude. Angew Chem Int Edit 42:2880–2883CrossRefGoogle Scholar
  188. 188.
    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 76:3999–4007CrossRefGoogle Scholar
  189. 189.
    Yi H, Nevin KP, Kim B-C, 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 24:3498–3503CrossRefGoogle Scholar
  190. 190.
    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 72:7345–7348CrossRefGoogle Scholar
  191. 191.
    Malvankar NS, Lovley DR (2012) Microbial nanowires, a new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5:1039–1046CrossRefGoogle Scholar
  192. 192.
    Meitl LA, Eggleston CM, Colberg PJS, Khare N, Reardon CL, Shi L (2009) Electrochemical interaction of Shewanella oneidensis MR-1 and its outer membrane cytochromes OmcA and MtrC with hematite electrodes. Geochim Cosmochim Ac 73:5292–5307CrossRefGoogle Scholar
  193. 193.
    Bouhenni RA, Vora GJ, Biffinger JC, Shirodkar S, Brockman K, Ray R, Wu P, Johnson BJ, Biddle EM, Marshall MJ, Fitzgerald LA, Little BJ, Fredrickson JK, Beliaev AS, Ringeisen BR, Saffarini DA (2010) The role of Shewanella oneidensis MR-1 outer surface structures in extracellular electron transfer. Electroanal 22:856–864CrossRefGoogle Scholar
  194. 194.
    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 Reports 3:211–217CrossRefGoogle Scholar
  195. 195.
    Busalmen JP, Esteve-Núñez A, Feliu JM (2008) Whole cell electrochemistry of electricity-producing microorganisms evidence an adaptation for optimal exocellular electron transport. Environ Sci Technol 42:2445–2450CrossRefGoogle Scholar
  196. 196.
    Fricke K, Harnisch F, Schröder U (2008) On the use of cyclic voltammetry for the study of anodic electron transfer in microbial fuel cells. Energ Environ Sci 1:144–147CrossRefGoogle Scholar
  197. 197.
    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. Electroanal 22:865–874CrossRefGoogle Scholar
  198. 198.
    Srikanth S, Marsili E, Flickinger MC, Bond DR (2008) Electrochemical characterization of Geobacter sulfurreducens cells immobilized on graphite paper electrodes. Biotechnol Bioeng 99:1065–1073CrossRefGoogle Scholar
  199. 199.
    Marsili E, Rollefson JB, Baron DB, Hozalski RM, Bond DR (2008) Microbial biofilm voltammetry: direct electrochemical characterization of catalytic electrode-attached biofilms. Appl Environ Microbiol 74:7329–7337CrossRefGoogle Scholar
  200. 200.
    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. Energ Environ Sci 2:506–516CrossRefGoogle Scholar
  201. 201.
    Strycharz-Glaven SM, Tender LM (2012) Study of the mechanism of catalytic activity of G. sulfurreducens biofilm anodes during biofilm growth. ChemSusChem 5:1106–1118CrossRefGoogle Scholar
  202. 202.
    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. Energ Environ Sci 4:896–913CrossRefGoogle Scholar
  203. 203.
    Zhu X, Yates MD, Logan BE (2012) Set potential regulation reveals additional oxidation peaks of Geobacter sulfurreducens anodic biofilms. Electrochem Commun 22:116–119CrossRefGoogle Scholar
  204. 204.
    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 8:1805–1815CrossRefGoogle Scholar
  205. 205.
    Nevin KP, Kim B-C, Glaven RH, Johnson JP, Woodard TL, Methé 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:e5628CrossRefGoogle Scholar
  206. 206.
    Kim B-C, 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 73:70–75CrossRefGoogle Scholar
  207. 207.
    Busalmen JP, Esteve-Nuñez A, Berná A, Feliu JM (2010) ATR-SEIRAs characterization of surface redox processes in G. sulfurreducens. Bioelectrochemistry 78:25–29CrossRefGoogle Scholar
  208. 208.
    Malvankar NS, Tuominen MT, Lovley DR (2012) Biofilm conductivity is a decisive variable for high-current-density Geobacter sulfurreducens microbial fuel cells. Energ Environ Sci 5:5790–5797CrossRefGoogle Scholar
  209. 209.
    Malvankar NS, Mester T, Tuominen MT, Lovley DR (2012) Supercapacitors based on c-type cytochromes using conductive nanostructured networks of living bacteria. Chemphyschem 13:463–468CrossRefGoogle Scholar
  210. 210.
    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 B-H, Fredrickson JK, Nealson KH (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73:7003–7012CrossRefGoogle Scholar
  211. 211.
    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 USA 106:22169–22174CrossRefGoogle Scholar
  212. 212.
    Okamoto A, Nakamura R, Hashimoto K (2011) In-vivo identification of direct electron transfer from Shewanella oneidensis MR-1 to electrodes via outer-membrane OmcA-MtrCAB protein complexes. Electrochim Acta 56:5526–5531CrossRefGoogle Scholar
  213. 213.
    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 284:28865–28873CrossRefGoogle Scholar
  214. 214.
    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 192:467–474CrossRefGoogle Scholar
  215. 215.
    Marritt SJ, Lowe TG, Bye J, McMillan DGG, Shi L, Fredrickson J, Zachara J, Richardson DJ, Cheesman MR, Jeuken LJC, Butt JN (2012) A functional description of CymA, an electron-transfer hub supporting anaerobic respiratory flexibility in Shewanella. Biochem J 444:465–474CrossRefGoogle Scholar
  216. 216.
    Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77:995–1008Google Scholar
  217. 217.
    Shi L, Chen B, Wang Z, Elias DA, Mayer MU, Gorby YA, Ni S, Lower BH, Kennedy DW, Wunschel DS, Mottaz HM, Marshall MJ, Hill EA, Beliaev AS, Zachara JM, Fredrickson JK, Squier T (2006) Isolation of a high-affinity functional protein complex between OmcA and MtrC: two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J Bacteriol 188:4705–4714CrossRefGoogle Scholar
  218. 218.
    Carmona-Martinez AA, Harnisch F, Fitzgerald LA, Biffinger JC, Ringeisen BR, Schröder U (2011) Cyclic voltammetric analysis of the electron transfer of Shewanella oneidensis MR-1 and nanofilament and cytochrome knock-out mutants. Bioelectrochemistry 81:74–80CrossRefGoogle Scholar
  219. 219.
    Nakamura R, Kai F, Okamoto A, Newton GJ, Hashimoto K (2009) Self-constructed electrically conductive bacterial networks. Angew Chem Int Edit 48:508–511CrossRefGoogle Scholar
  220. 220.
    Jain A, Zhang X, Pastorella G, Connolly JO, Barry N, Woolley R, Krishnamurthy S, Marsili E (2012) Electron transfer mechanism in Shewanella loihica PV-4 biofilms formed at graphite electrode. Bioelectrochemistry 87:28–32CrossRefGoogle Scholar
  221. 221.
    Newton GJ, Mori S, Nakamura R, Hashimoto K, Watanabe K (2009) Analyses of current-generation mechanisms of Shewanella loihica PV-4 in microbial fuel cells in comparison with Shewanella oneidensis MR-1. Appl Environ Microbiol 75:7674–7681CrossRefGoogle Scholar
  222. 222.
    Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim B-C, Inoue K, Mester T, Covalla SF, Johnson JP, Rotello VM, Tuominen MT, Lovley DR (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nano 6:573–579CrossRefGoogle Scholar
  223. 223.
    Malvankar NS, Lau J, Nevin KP, Franks AE, Tuominen MT, Lovley DR (2012) Electrical conductivity in a mixed-species biofilm. Appl Environ Microbiol. doi: 10.1128/AEM.01803-12
  224. 224.
    Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM (2011) On the electrical conductivity of microbial nanowires and biofilms. Energ Environ Sci 4:4366–4379CrossRefGoogle Scholar
  225. 225.
    Magnuson TS (2011) How the xap locus put electrical “Zap” in Geobacter sulfurreducens biofilms. J Bacteriol 193(5):1021–1022CrossRefGoogle Scholar
  226. 226.
    Cao B, Shi L, Brown RN, Xiong Y, Fredrickson JK, Romine MF, Marshall MJ, Lipton MS, Beyenal H (2011) Extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms: characterization by infrared spectroscopy and proteomics. Environ Microbiol 13:1018–1031CrossRefGoogle Scholar
  227. 227.
    Leang C, Qian X, Mester TN, Lovley DR (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl Environ Microbiol 76:4080–4084CrossRefGoogle Scholar
  228. 228.
    Lovley DR (2012) Electromicrobiology. Annu Rev Microbiol 66:391–409CrossRefGoogle Scholar
  229. 229.
    Malvankar NS, Tuominen MT, Lovley DR (2012) Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens. Energ Environ Sci 5:8651–8659CrossRefGoogle Scholar
  230. 230.
    Veazey JP, Reguera G, Tessmer SH (2011) Electronic properties of conductive pili of the metal-reducing bacterium Geobacter sulfurreducens probed by scanning tunneling microscopy. Phys Rev E 84:060901CrossRefGoogle Scholar
  231. 231.
    Bond DR, Strycharz-Glaven SM, Tender LM, Torres CI (2012) On electron transport through Geobacter biofilms. ChemSusChem 5:1099–1105CrossRefGoogle Scholar
  232. 232.
    Schrott GD, Bonanni PS, Robuschi L, Esteve-Núñez A, Busalmen JP (2011) Electrochemical insight into the mechanism of electron transport in biofilms of Geobacter sulfurreducens. Electrochim Acta 56:10791–10795CrossRefGoogle Scholar
  233. 233.
    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 193:1023–1033CrossRefGoogle Scholar
  234. 234.
    Malvankar NS, Tuominen MT, Lovley DR (2012) Comment on “On electrical conductivity of microbial nanowires and biofilms” by Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM (2011) Energ Environ Sci 4:4366". Energ Environ Sci 5:6247–6249CrossRefGoogle Scholar
  235. 235.
    Strycharz-Glaven SM, Tender LM (2012) Reply to the ‘Comment on “On electrical conductivity of microbial nanowires and biofilms” by Malvankar NS, Tuominen MT, Lovley DR (2012) Energ Environ Sci 5:6247–6249’. Energ Environ Sci 5:6250–6255CrossRefGoogle Scholar
  236. 236.
    Polizzi NF, Skourtis SS, Beratan DN (2012) Physical constraints on charge transport through bacterial nanowires. Faraday Discuss 155:43–61CrossRefGoogle Scholar
  237. 237.
    Fitzgerald LA, Petersen ER, Ray RI, Little BJ, Cooper CJ, Howard EC, Ringeisen BR, Biffinger JC (2012) Shewanella oneidensis MR-1 Msh pilin proteins are involved in extracellular electron transfer in microbial fuel cells. Process Biochem 47:170–174CrossRefGoogle Scholar
  238. 238.
    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 76:4151–4157CrossRefGoogle Scholar
  239. 239.
    Jiang X, Hu J, Fitzgerald LA, Biffinger JC, Xie P, Ringeisen BR, Lieber CM (2010) Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging. Proc Natl Acad Sci USA 107:16806–16810CrossRefGoogle Scholar
  240. 240.
    Biffinger JC, Fitzgerald LA, Ray R, Little BJ, Lizewski SE, Petersen ER, Ringeisen BR, Sanders WC, Sheehan PE, Pietron JJ, Baldwin JW, Nadeau LJ, Johnson GR, Ribbens M, Finkel SE, Nealson KH (2011) The utility of Shewanella japonica for microbial fuel cells. Bioresource Technol 102:290–297CrossRefGoogle Scholar
  241. 241.
    Yang Y, Sun G, Guo J, Xu M (2011) Differential biofilms characteristics of Shewanella decolorationis microbial fuel cells under open and closed circuit conditions. Bioresource Technol 102:7093–7098CrossRefGoogle Scholar
  242. 242.
    Li S-L, Freguia S, Liu S-M, Cheng S-S, Tsujimura S, Shirai O, Kano K (2010) Effects of oxygen on Shewanella decolorationis NTOU1 electron transfer to carbon-felt electrodes. Biosens Bioelectron 25:2651–2656CrossRefGoogle Scholar
  243. 243.
    Borole AP, Reguera G, Ringeisen B, Wang Z-W, Feng Y, Kim BH (2011) Electroactive biofilms: current status and future research needs. Energ Environ Sci 4:4813–4834CrossRefGoogle Scholar
  244. 244.
    Holmes DE, Bond DR, Lovley DR (2004) Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl Environ Microbiol 70:1234–1237CrossRefGoogle Scholar
  245. 245.
    Marshall CW, May HD (2009) Electrochemical evidence of direct electrode reduction by a thermophilic Gram-positive bacterium, Thermincola ferriacetica. Energ Environ Sci 2:699–705CrossRefGoogle Scholar
  246. 246.
    Zhuang L, Zhou S, Yuan Y, Liu T, Wu Z, Cheng J (2011) Development of Enterobacter aerogenes fuel cells: from in situ biohydrogen oxidization to direct electroactive biofilm. Bioresource Technol 102:284–289CrossRefGoogle Scholar
  247. 247.
    Wrighton KC, Thrash JC, Melnyk RA, Bigi JP, Byrne-Bailey KG, Remis JP, Schichnes D, Auer M, Chang CJ, Coates JD (2011) Evidence for direct electron transfer by a Gram-positive bacterium isolated from a microbial fuel cell. Appl Environ Microbiol 77:7633–7639CrossRefGoogle Scholar
  248. 248.
    Carlson HK, Iavarone AT, Gorur A, Yeo BS, Tran R, Melnyk RA, Mathies RA, Auer M, Coates JD (2012) Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria. Proc Natl Acad Sci USA 109:1702–1707CrossRefGoogle Scholar
  249. 249.
    Masuda M, Freguia S, Wang Y-F, Tsujimura S, Kano K (2010) Flavins contained in yeast extract are exploited for anodic electron transfer by Lactococcus lactis. Bioelectrochemistry 78:173–175CrossRefGoogle Scholar
  250. 250.
    Velasquez-Orta S, Head I, Curtis T, Scott K, Lloyd J, von Canstein H (2010) The effect of flavin electron shuttles in microbial fuel cells current production. Appl Microbiol Biot 85:1373–1381CrossRefGoogle Scholar
  251. 251.
    Zhang T, Zhang L, Su W, Gao P, Li D, He X, Zhang Y (2011) The direct electrocatalysis of phenazine-1-carboxylic acid excreted by Pseudomonas alcaliphila under alkaline condition in microbial fuel cells. Bioresource Technol 102(14):7099–7102CrossRefGoogle Scholar
  252. 252.
    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 76:14–18CrossRefGoogle Scholar
  253. 253.
    Qiao Y, Li CM, Bao SJ, Lu ZS, Hong YH (2008) Direct electrochemistry and electrocatalytic mechanism of evolved Escherichia coli cells in microbial fuel cells. Chem Commun 11:1290–1292CrossRefGoogle Scholar
  254. 254.
    Bond DR, Lovley DR (2005) Evidence for involvement of an electron shuttle in electricity generation by Geothrix fermentans. Appl Environ Microbiol 71:2186–2189CrossRefGoogle Scholar
  255. 255.
    Venkataraman A, Rosenbaum MA, Perkins SD, Werner JJ, Angenent LT (2011) Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems. Energ Environ Sci 4:4550–4559CrossRefGoogle Scholar
  256. 256.
    Kim N, Choi Y, Jung S, Kim S (2000) Development of microbial fuel cells using Proteus vulgaris. B Korean Chem Soc 21:44–48Google Scholar
  257. 257.
    Thurston CF, Bennetto HP, Delaney GM, Mason JR, Roller SD, Stirling JL (1985) Glucose metabolism in a microbial fuel cell: stoichiometry of product formation in a thionine-mediated Proteus vulgaris fuel cell and its relation to coulombic yields. J Gen Microbiol 131:1393–1401Google Scholar
  258. 258.
    Wen Q, Kong F, Ma F, Ren Y, Pan Z (2011) Improved performance of air-cathode microbial fuel cell through additional Tween 80. J Power Sources 196:899–904CrossRefGoogle Scholar
  259. 259.
    Ho PI, Kumar GG, Kim AR, Kim P, Nahm KS (2011) Microbial electricity generation of diversified carbonaceous electrodes under variable mediators. Bioelectrochemistry 80:99–104CrossRefGoogle Scholar
  260. 260.
    Wen Q, Kong F, Ren Y, Cao D, Wang G, Zheng H (2010) Improved performance of microbial fuel cell through addition of rhamnolipid. Electrochem Commun 12:1710–1713CrossRefGoogle Scholar
  261. 261.
    Schröder U (2007) Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency. Phys Chem Chem Phys 9:2619–2629CrossRefGoogle Scholar
  262. 262.
    Kimmel DW, LeBlanc G, Meschievitz ME, Cliffel DE (2011) Electrochemical sensors and biosensors. Anal Chem 84:685–707CrossRefGoogle Scholar
  263. 263.
    Eltzov E, Marks R (2011) Whole-cell aquatic biosensors. Anal Bioanal Chem 400:895–913CrossRefGoogle Scholar
  264. 264.
    Xu F, Duan J, Hou B (2010) Electron transfer process from marine biofilms to graphite electrodes in seawater. Bioelectrochemistry 78:92–95CrossRefGoogle Scholar
  265. 265.
    Qiao Y, Bao S-J, Li CM (2010) Electrocatalysis in microbial fuel cells-from electrode material to direct electrochemistry. Energ Environ Sci 3(5):544–553CrossRefGoogle Scholar
  266. 266.
    Hasan K, Patil SA, Górecki K, Leech D, Hägerhäll C, Gorton L (2012) Electrochemical communication between heterotrophically grown Rhodobacter capsulatus with electrodes mediated by an osmium redox polymer. Bioelectrochemistry. doi: 10.1016/j.bioelechem.2012.1005.1004
  267. 267.
    Rawson FJ, Garrett DJ, Leech D, Downard AJ, Baronian KHR (2011) Electron transfer from Proteus vulgaris to a covalently assembled, single walled carbon nanotube electrode functionalised with osmium bipyridine complex: application to a whole cell biosensor. Biosens Bioelectron 26:2383–2389CrossRefGoogle Scholar
  268. 268.
    Hasan K, Patil SA, Leech D, Hägerhäll C, Gorton L (2012) Electrochemical communication between microbial cells and electrodes via osmium redox systems. Biochem Soc T 40(6):1330–1335Google Scholar
  269. 269.
    Niessen J, Schröder U, Harnisch F, Scholz F (2005) Gaining electricity from in situ oxidation of hydrogen produced by fermentative cellulose degradation. Lett Appl Microbiol 41:286–290CrossRefGoogle Scholar
  270. 270.
    Niessen J, Schröder U, Scholz F (2004) Exploiting complex carbohydrates for microbial electricity generation: a bacterial fuel cell operating on starch. Electrochem Commun 6:955–958CrossRefGoogle Scholar
  271. 271.
    Karube I, Matsunaga T, Tsuru S, Suzuki S (1977) Biochemical fuel cell utilizing immobilized cells of Clostridium butyricum. Biotechnol Bioeng 19:1727–1733CrossRefGoogle Scholar
  272. 272.
    Velasquez-Orta SB, Head IM, Curtis TP, Scott K (2011) Factors affecting current production in microbial fuel cells using different industrial wastewaters. Bioresource Technol 102:5105–5112CrossRefGoogle Scholar
  273. 273.
    Ren Z, Yan H, Wang W, Mench MM, Regan JM (2011) Characterization of microbial fuel cells at microbially and electrochemically meaningful time scales. Environ Sci Technol 45:2435–2441CrossRefGoogle Scholar
  274. 274.
    Harnisch F, Koch C, Patil SA, Hübschmann T, Müller S, Schröder U (2011) Revealing the electrochemically driven selection in natural community derived microbial biofilms using flow-cytometry. Energ Environ Sci 4:1265–1267CrossRefGoogle Scholar
  275. 275.
    Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485CrossRefGoogle Scholar
  276. 276.
    Patil SA, Hasan K, Leech D, Hägerhäll C, Gorton L (2012) Improved microbial electrocatalysis with osmium polymer modified electrodes. Chem Commun 48:10183–10185CrossRefGoogle Scholar
  277. 277.
    Gregory KB, Lovley DR (2005) Remediation and recovery of uranium from contaminated subsurface environments with electrodes. Environ Sci Technol 39:8943–8947CrossRefGoogle Scholar
  278. 278.
    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 80:142–150CrossRefGoogle Scholar
  279. 279.
    Strycharz SM, Woodard TL, Johnson JP, Nevin KP, Sanford RA, Löffler FE, Lovley DR (2008) Graphite electrode as a sole electron donor for reductive dechlorination of tetrachlorethene by Geobacter lovleyi. Appl Environ Microbiol 74:5943–5947CrossRefGoogle Scholar
  280. 280.
    Strik DPBTB, Hamelers HVM, Buisman CJN (2009) Solar energy powered microbial fuel cell with a reversible bioelectrode. Environ Sci Technol 44:532–537CrossRefGoogle Scholar
  281. 281.
    Parot S, Vandecandelaere I, Cournet A, Délia M-L, Vandamme P, Bergé M, Roques C, Bergel A (2011) Catalysis of the electrochemical reduction of oxygen by bacteria isolated from electro-active biofilms formed in seawater. Bioresource Technol 102:304–311CrossRefGoogle Scholar
  282. 282.
    You SJ, Ren NQ, Zhao QL, Wang JY, Yang FL (2009) Power generation and electrochemical analysis of biocathode microbial fuel cell using graphite fibre brush as cathode material. Fuel Cells 9:588–596CrossRefGoogle Scholar
  283. 283.
    Vandecandelaere I, Nercessian O, Faimali M, Segaert E, Mollica A, Achouak W, De Vos P, Vandamme P (2010) Bacterial diversity of the cultivable fraction of a marine electroactive biofilm. Bioelectrochemistry 78:62–66CrossRefGoogle Scholar
  284. 284.
    Freguia S, Tsujimura S, Kano K (2010) Electron transfer pathways in microbial oxygen biocathodes. Electrochim Acta 55:813–818CrossRefGoogle Scholar
  285. 285.
    Aulenta F, Catervi A, Majone M, Panero S, Reale P, Rossetti S (2007) Electron transfer from a solid-state electrode assisted by methyl viologen sustains efficient microbial reductive dechlorination of TCE. Environ Sci Technol 41:2554–2559CrossRefGoogle Scholar
  286. 286.
    Park DH, Zeikus JG (1999) Utilization of electrically reduced neutral red by Actinobacillus succinogenes: physiological function of neutral red in membrane-driven fumarate reduction and energy conservation. J Bacteriol 181:2403–2410Google Scholar
  287. 287.
    Emde R, Schink B (1990) Enhanced propionate formation by Propionibacterium freudenreichii subsp. freudenreichii in a three-electrode amperometric culture system. Appl Environ Microbiol 56:2771–2776Google Scholar
  288. 288.
    Shin HS, Jain MJ, Chartrain MC, Zeikus JZ (2001) Evaluation of an electrochemical bioreactor system in the biotransformation of 6-bromo-2-tetralone to 6-bromo-2-tetralol. Appl Microbiol Biot 57(4):506–510CrossRefGoogle Scholar
  289. 289.
    Hongo M, Iwahara M (1979) Determination of electro-energizing conditions for l-glutamic acid fermentation. Agric Biol Chem 43:2083–2086CrossRefGoogle Scholar
  290. 290.
    Steinbusch KJJ, Hamelers HVM, Schaap JD, Kampman C, Buisman CJN (2009) Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. Environ Sci Technol 44:513–517CrossRefGoogle Scholar
  291. 291.
    Aulenta F, Canosa A, Majone M, Panero S, Reale P, Rossetti S (2008) Trichloroethene dechlorination and H2 evolution are alternative biological pathways of electric charge utilization by a dechlorinating culture in a bioelectrochemical system. Environ Sci Technol 42:6185–6190CrossRefGoogle Scholar
  292. 292.
    Thrash JC, Van Trump JI, Weber KA, Miller E, Achenbach LA, Coates JD (2007) Electrochemical stimulation of microbial perchlorate reduction. Environ Sci Technol 41:1740–1746CrossRefGoogle Scholar
  293. 293.
    Lojou E, Durand MC, Dolla A, Bianco P (2002) Hydrogenase activity control at Desulfovibrio vulgaris cell-coated carbon electrodes: biochemical and chemical factors influencing the mediated bioelectrocatalysis. Electroanal 14:913–922CrossRefGoogle Scholar
  294. 294.
    Aulenta F, Reale P, Canosa A, Rossetti S, Panero S, Majone M (2010) Characterization of an electro-active biocathode capable of dechlorinating trichloroethene and cis-dichloroethene to ethene. Biosens Bioelectron 25:1796–1802CrossRefGoogle Scholar
  295. 295.
    Aulenta F, Canosa A, Reale P, Rossetti S, Panero S, Majone M (2009) Microbial reductive dechlorination of trichloroethene to ethene with electrodes serving as electron donors without the external addition of redox mediators. Biotechnol Bioeng 103:85–91CrossRefGoogle Scholar
  296. 296.
    Sakakibara Y, Kuroda M (1993) Electric prompting and control of denitrification. Biotechnol Bioeng 42:535–537CrossRefGoogle Scholar
  297. 297.
    Park HI, Dk K, Choi Y-J, Pak D (2005) Nitrate reduction using an electrode as direct electron donor in a biofilm-electrode reactor. Process Biochem 40:3383–3388CrossRefGoogle Scholar
  298. 298.
    Feleke Z, Araki K, Sakakibara Y, Watanabe T, Kuroda M (1998) Selective reduction of nitrate to nitrogen gas in a biofilm-electrode reactor. Water Res 32:2728–2734CrossRefGoogle Scholar
  299. 299.
    Cast KL, Flora JRV (1998) An evaluation of two cathode materials and the impact of copper on bioelectrochemical denitrification. Water Res 32:63–70CrossRefGoogle Scholar
  300. 300.
    Rabaey K, Girguis P, Nielsen LK (2011) Metabolic and practical considerations on microbial electrosynthesis. Curr Opin Biotech 22:371–377CrossRefGoogle Scholar
  301. 301.
    Zhao F, Slade RCT, Varcoe JR (2009) Techniques for the study and development of microbial fuel cells: an electrochemical perspective. Chem Soc Rev 38(7):1926–1939CrossRefGoogle Scholar
  302. 302.
    He Z, Mansfeld F (2009) Exploring the use of electrochemical impedance spectroscopy (EIS) in microbial fuel cell studies. Energ Environ Sci 2:215–219CrossRefGoogle Scholar
  303. 303.
    Watson VJ, Logan BE (2011) Analysis of polarization methods for elimination of power overshoot in microbial fuel cells. Electrochem Commun 13:54–56CrossRefGoogle Scholar
  304. 304.
    Manohar AK, Bretschger O, Nealson KH, Mansfeld F (2008) The polarization behavior of the anode in a microbial fuel cell. Electrochim Acta 53:3508–3513CrossRefGoogle Scholar
  305. 305.
    Patil SA, Harnisch F, Koch C, Hübschmann T, Fetzer I, Carmona-Martinez AA, Müller S, Schröder U (2011) Electroactive mixed culture derived biofilms in microbial bioelectrochemical systems: the role of pH on biofilm formation, performance and composition. Bioresource Technol 102:9683–9690CrossRefGoogle Scholar
  306. 306.
    Chen S, Hou H, Harnisch F, Patil SA, Carmona-Martinez AA, Agarwal S, Zhang Y, Sinha-Ray S, Yarin AL, Greiner A, Schröder U (2011) Electrospun and solution blown three-dimensional carbon fiber nonwovens for application as electrodes in microbial fuel cells. Energ Environ Sci 4:1417–1421CrossRefGoogle Scholar
  307. 307.
    Patil SA, Harnisch F, Kapadnis B, Schröder U (2010) Electroactive mixed culture biofilms in microbial bioelectrochemical systems: the role of temperature for biofilm formation and performance. Biosens Bioelectron 26:803–808CrossRefGoogle Scholar
  308. 308.
    Liu Y, Harnisch F, Fricke K, Sietmann R, Schröder U (2008) Improvement of the anodic bioelectrocatalytic activity of mixed culture biofilms by a simple consecutive electrochemical selection procedure. Biosens Bioelectron 24:1006–1011CrossRefGoogle Scholar
  309. 309.
    Torres CI, Krajmalnik-Brown R, Parameswaran P, Marcus AK, Wanger G, Gorby YA, Rittmann BE (2009) Selecting anode-respiring bacteria based on anode potential: phylogenetic, electrochemical, and microscopic characterization. Environ Sci Technol 43:9519–9524CrossRefGoogle Scholar
  310. 310.
    Pocaznoi D, Erable B, Delia M-L, Bergel A (2012) Ultra microelectrodes increase the current density provided by electroactive biofilms by improving their electron transport ability. Energ Environ Sci 5:5287–5296CrossRefGoogle Scholar
  311. 311.
    Parot S, Délia M-L, Bergel A (2008) Forming electrochemically active biofilms from garden compost under chronoamperometry. Bioresource Technol 99:4809–4816CrossRefGoogle Scholar
  312. 312.
    Wei J, Liang P, Cao X, Huang X (2010) A new insight into potential regulation on growth and power generation of Geobacter sulfurreducens in microbial fuel cells based on energy viewpoint. Environ Sci Technol 44:3187–3191CrossRefGoogle Scholar
  313. 313.
    Aelterman P, Freguia S, Keller J, Verstraete W, Rabaey K (2008) The anode potential regulates bacterial activity in microbial fuel cells. Appl Microbiol Biot 78:409–418CrossRefGoogle Scholar
  314. 314.
    Finkelstein DA, Tender LM, Zeikus JG (2006) Effect of electrode potential on electrode-reducing microbiota. Environ Sci Technol 40:6990–6995CrossRefGoogle Scholar
  315. 315.
    Cheng KY, Ho G, Cord-Ruwisch R (2008) Affinity of microbial fuel cell biofilm for the anodic potential. Environ Sci Technol 42:3828–3834CrossRefGoogle Scholar
  316. 316.
    Wagner RC, Call DF, Logan BE (2010) Optimal set anode potentials vary in bioelectrochemical systems. Environ Sci Technol 44:6036–6041CrossRefGoogle Scholar
  317. 317.
    Pocaznoi D, Erable B, Etcheverry L, Delia M-L, Bergel A (2012) Forming microbial anodes under delayed polarisation modifies the electron transfer network and decreases the polarisation time required. Bioresource Technol 114:334–341CrossRefGoogle Scholar
  318. 318.
    Harnisch F, Freguia S (2012) A basic tutorial on cyclic voltammetry for the investigation of electroactive microbial biofilms. Chem Asian J 7:466–475CrossRefGoogle Scholar
  319. 319.
    Torres CI, Marcus AK, Lee H-S, Parameswaran P, Krajmalnik-Brown R, Rittmann BE (2010) A kinetic perspective on extracellular electron transfer by anode-respiring bacteria. FEMS Microbiol Rev 34:3–17CrossRefGoogle Scholar
  320. 320.
    Park HS, Kim BH, Kim HS, Kim HJ, Kim GT, Kim M, Chang IS, Park YK, Chang HI (2001) A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Clostridium butyricum isolated from a microbial fuel cell. Anaerobe 7:297–306CrossRefGoogle Scholar
  321. 321.
    Zhang T, Cui C, Chen S, Ai X, Yang H, Shen P, Peng Z (2006) A novel mediatorless microbial fuel cell based on direct biocatalysis of Escherichia coli. Chem Commun 21:2257–2259CrossRefGoogle Scholar
  322. 322.
    Kim HJ, Park HS, Hyun MS, Chang IS, Kim M, Kim BH (2002) A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens. Enzyme Microb Tech 30:145–152CrossRefGoogle Scholar
  323. 323.
    Rabaey K, Ossieur W, Verhaege M, Verstraete W (2005) Continuous microbial fuel cells convert carbohydrates to electricity. Water Sci Technol 52:515–523Google Scholar
  324. 324.
    Yoon SM, Choi CH, Kim M, Hyun MS, Shin SH, Yi D, Kim HJ (2007) Enrichment of electrochemically active bacteria using a three-electrode electrochemical cell. J Microbiol Biotechnol 17:110–115Google Scholar
  325. 325.
    He Z, Minteer SD, Angenent LT (2005) Electricity generation from artificial wastewater using an upflow microbial fuel cell. Environ Sci Technol 39:5262–5267CrossRefGoogle Scholar
  326. 326.
    Pham CA, Jung SJ, Phung NT, Lee J, Chang IS, Kim BH, Yi H, Chun J (2003) A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Aeromonas hydrophila, isolated from a microbial fuel cell. FEMS Microbiol Lett 223:129–134CrossRefGoogle Scholar
  327. 327.
    Liu H, Cheng S, Logan BE (2004) Production of electricity from acetate or butyrate using a single-chamber microbial fuel cell. Environ Sci Technol 39:658–662CrossRefGoogle Scholar
  328. 328.
    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 70:5373–5382CrossRefGoogle Scholar
  329. 329.
    Katuri KP, Kavanagh P, Rengaraj S, Leech D (2010) Geobacter sulfurreducens biofilms developed under different growth conditions on glassy carbon electrodes: insights using cyclic voltammetry. Chem Commun 46:4758–4760CrossRefGoogle Scholar
  330. 330.
    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 56:10776–10785CrossRefGoogle Scholar
  331. 331.
    Liu H, Newton GJ, Nakamura R, Hashimoto K, Nakanishi S (2010) Electrochemical characterization of a single electricity-producing bacterial cell of Shewanella by using optical tweezers. Angew Chem Int Edit 49:6596–6599CrossRefGoogle Scholar
  332. 332.
    Okamoto A, Nakamura R, Ishii K, Hashimoto K (2009) In vivo electrochemistry of C-type cytochrome-mediated electron-transfer with chemical marking. Chembiochem 10:2329–2332CrossRefGoogle Scholar
  333. 333.
    Katuri KP, Rengaraj S, Kavanagh P, O’Flaherty V, Leech D (2012) Charge transport through Geobacter sulfurreducens biofilms grown on graphite rods. Langmuir 28:7904–7913CrossRefGoogle Scholar
  334. 334.
    Wu X, Zhao F, Rahunen N, Varcoe JR, Avignone-Rossa C, Thumser AE, Slade RCT (2011) A role for microbial palladium nanoparticles in extracellular electron transfer. Angew Chem Int Edit 50:427–430CrossRefGoogle Scholar
  335. 335.
    Millo D, Harnisch F, Patil SA, Ly HK, Schröder U, Hildebrandt P (2011) In situ spectroelectrochemical investigation of electrocatalytic microbial biofilms by surface-enhanced resonance Raman spectroscopy. Angew Chem Int Edit 50:2625–2627CrossRefGoogle Scholar
  336. 336.
    Liu Y, Kim H, Franklin RR, Bond DR (2011) Linking spectral and electrochemical analysis to monitor c-type cytochrome redox status in living Geobacter sulfurreducens biofilms. Chemphyschem 12:2235–2241CrossRefGoogle Scholar
  337. 337.
    Busalmen JP, Berná A, Feliu JM (2007) Spectroelectrochemical examination of the interaction between bacterial cells and gold electrodes. Langmuir 23:6459–6466CrossRefGoogle Scholar
  338. 338.
    Nakamura R, Ishii K, Hashimoto K (2009) Electronic absorption spectra and redox properties of c type cytochromes in living microbes. Angew Chem Int Edit 48:1606–1608CrossRefGoogle Scholar
  339. 339.
    Liu Y, Bond DR (2012) Long-distance electron transfer by G. sulfurreducens biofilms results in accumulation of reduced c-type cytochromes. ChemSusChem 5:1047–1053CrossRefGoogle Scholar
  340. 340.
    Biju V, Pan D, Gorby YA, Fredrickson J, McLean J, Saffarini D, Lu HP (2006) Combined spectroscopic and topographic characterization of nanoscale domains and their distributions of a redox protein on bacterial cell surfaces. Langmuir 23:1333–1338CrossRefGoogle Scholar
  341. 341.
    Compton RG, Perkin SJ, Gamblin DP, Davis J, Marken F, Padden AN, John P (2000) Clostridium isatidis colonised carbon electrodes: voltammetric evidence for direct solid state redox processes. New J Chem 24:179–181CrossRefGoogle Scholar
  342. 342.
    Parot S, Nercessian O, Délia ML, Achouak W, Bergel A (2009) Electrochemical checking of aerobic isolates from electrochemically active biofilms formed in compost. J Appl Microbiol 106:1350–1359CrossRefGoogle Scholar
  343. 343.
    Dominguez-Benetton X, Sevda S, Vanbroekhoven K, Pant D (2012) The accurate use of impedance analysis for the study of microbial electrochemical systems. Chem Soc Rev 41:7228–7246CrossRefGoogle Scholar
  344. 344.
    Strik DP, Ter Heijne A, Hamelers HVM, Saakes M, Buisman C (2008) Feasibility study on electrochemical impedance spectroscopy for microbial fuel cells: measurement modes & data validation. ECS Trans 13:27–41CrossRefGoogle Scholar
  345. 345.
    He Z, Wagner N, Minteer SD, Angenent LT (2006) An upflow microbial fuel cell with an interior cathode: assessment of the internal resistance by impedance spectroscopy. Environ Sci Technol 40:5212–5217CrossRefGoogle Scholar
  346. 346.
    Ouitrakul S, Sriyudthsak M, Charojrochkul S, Kakizono T (2007) Impedance analysis of bio-fuel cell electrodes. Biosens Bioelectron 23:721–727CrossRefGoogle Scholar
  347. 347.
    Ramasamy RP, Ren Z, Mench MM, Regan JM (2008) Impact of initial biofilm growth on the anode impedance of microbial fuel cells. Biotechnol Bioeng 101:101–108CrossRefGoogle Scholar
  348. 348.
    Borole AP, Aaron D, Hamilton CY, Tsouris C (2010) Understanding long-term changes in microbial fuel cell performance using electrochemical impedance spectroscopy. Environ Sci Technol 44:2740–2745CrossRefGoogle Scholar
  349. 349.
    Aaron D, Tsouris C, Hamilton CY, Borole AP (2010) Assessment of the effects of flow rate and ionic strength on the performance of an air-cathode microbial fuel cell using electrochemical impedance spectroscopy. Energies 3:592–606CrossRefGoogle Scholar
  350. 350.
    He Z, Huang Y, Manohar AK, Mansfeld F (2008) Effect of electrolyte pH on the rate of the anodic and cathodic reactions in an air-cathode microbial fuel cell. Bioelectrochemistry 74:78–82CrossRefGoogle Scholar
  351. 351.
    ter Heijne A, Schaetzle O, Gimenez S, Fabregat-Santiago F, Bisquert J, Strik DPBTB, Barriere F, Buisman CJN, Hamelers HVM (2011) Identifying charge and mass transfer resistances of an oxygen reducing biocathode. Energ Environ Sci 4:5035–5043CrossRefGoogle Scholar
  352. 352.
    Virdis B, Harnisch F, Batstone DJ, Rabaey K, Donose BC (2012) Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy. Energ Environ Sci 5:7017–7024CrossRefGoogle Scholar
  353. 353.
    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 3:344–348CrossRefGoogle Scholar
  354. 354.
    Franks AE, Glaven RH, Lovley DR (2012) Real-time spatial gene expression analysis within current-producing biofilms. ChemSusChem 5:1092–1098CrossRefGoogle Scholar
  355. 355.
    Harnisch F, Rabaey K (2012) The diversity of techniques to study electrochemically active biofilms highlights the need for standardization. ChemSusChem 5:1027–1038CrossRefGoogle Scholar
  356. 356.
    Clarke TA, Edwards MJ, Gates AJ, Hall A, White GF, Bradley J, Reardon CL, Shi L, Beliaev AS, Marshall MJ, Wang Z, Watmough NJ, Fredrickson JK, Zachara JM, Butt JN, Richardson DJ (2011) Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci USA 108:9384–9389CrossRefGoogle Scholar
  357. 357.
    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 330:1413–1415CrossRefGoogle Scholar
  358. 358.
    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(4):e00159–11CrossRefGoogle Scholar
  359. 359.
    Rotaru A-E, Shrestha PM, Liu F, Ueki T, Nevin K, Summers ZM, Lovley DR (2012) Interspecies electron transfer via H2 and formate rather than direct electrical connections in co-cultures of Pelobacter carbinolicus and Geobacter sulfurreducens. Appl Environ Microbiol 78(21):7645–7651Google Scholar
  360. 360.
    Pfeffer C, Larsen S, Song J, Dong M, Besenbacher F, Meyer RL, Kjeldsen KU, Schreiber L, Gorby YA, El-Naggar MY, Leung KM, Schramm A, Risgaard-Petersen N, Nielsen LP (2012) Filamentous bacteria transport electrons over centimetre distances. Nature 491:218–221Google Scholar

Copyright information

© Springer-Verlag Wien 2012

Authors and Affiliations

  • Sunil A. Patil
    • 1
    Email author
  • Cecilia Hägerhäll
    • 1
  • Lo Gorton
    • 1
  1. 1.Department of Biochemistry and Structural Biology, Center for Molecular Protein ScienceLund UniversityLundSweden

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