Skip to main content
SpringerLink
Log in

Anaerobes in Bioelectrochemical Systems

  • Chapter
  • First Online:
Anaerobes in Biotechnology

Part of the book series: Advances in Biochemical Engineering/Biotechnology ((ABE,volume 156))

Abstract

In bioelectrochemical systems (BES), the catalytic activity of anaerobic microorganisms generates electrons at the anode which can be used, for example, for the production of electricity or chemical compounds. BES can be used for various purposes, including wastewater treatment, production of electricity, fuels and chemicals, biosensors, bioremediation, and desalination. Electrochemically active microorganisms are widely present in the environment and they can be found, in sediment, soil, compost, wastewaters and their treatment plants. Exoelectrogens are microorganisms capable of donating electrons to anode electrode or accepting electrons from cathode electrode and are mainly responsible for current generation or use in BES. However, current generation from fermentable substrates often requires the presence of electrochemically inactive microorganisms that break down complex substrates into metabolites which can be further utilized by exoelectrogens. The growth and electron transfer efficiency of anaerobes depend on several parameters, such as system architecture, electrode material and porosity, electrode potential and external resistance, pH, temperature, substrate concentration, organic loading rate, and ionic strength. In this chapter, the principles and microbiology of bioelectrochemical systems as well as selective factors for exoelectrogens are reviewed. The anaerobic microorganisms and their electron transfer mechanisms at the anode and cathode are described and future aspects are briefly discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

BES:

Bioelectrochemical system

BOD:

Biological oxygen demand

CE:

Coulombic efficiency

MDC:

Microbial desalination cell

MEC:

Microbial electrolysis cell

MES:

Microbial electrosynthesis

MFC:

Microbial fuel cell

OLR:

Organic loading rate

VFA:

Volatile fatty acid

References

  1. He Z, Angenent LT (2006) Application of bacterial biocathodes in microbial fuel cells. Electroanalysis 18:2009–2015

    Article  CAS  Google Scholar 

  2. 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 102:324–333

    Article  CAS  Google Scholar 

  3. Lapinsonniére L, Picot M, Barriére F (2012) Enzymatic versus microbial bio-catalyzed electrodes in bio-electrochemical systems. ChemSusChem 5:995–1005

    Article  CAS  Google Scholar 

  4. Rubenwolf S, Kerzenmacher S, Zengerle R, von Stetten F (2011) Strategies to extend the lifetime of bioelectrochemical enzyme electrodes for biosensing and biofuel cell applications. Appl Microbiol Biotechnol 89:1315–1322

    Article  CAS  Google Scholar 

  5. Logan BE, Regan JM (2006) Electricity-producing bacterial communities in microbial fuel cells. Trends Microbiol 14:512–518

    Article  CAS  Google Scholar 

  6. Rozendal RA, Hamelers HVM, Rabaey K, Keller J, Buisman CJN (2008) Towards practical implementation of bioelectrochemical wastewater treatment. Trends Biotechnol 26:450–459

    Article  CAS  Google Scholar 

  7. Rabaey K, Lissens G, Siciliano SD, Verstraete W (2003) A microbial fuel cell capable of converting glucose to electricity at high rate and efficiency. Biotechnol Lett 25:1531–1535

    Google Scholar 

  8. 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 41:3354–3360

    Article  CAS  Google Scholar 

  9. Lefebvre O, Al-Mamun A, Ng HY (2008) A microbial fuel cell equipped with a biocathode for organic removal and denitrification. Water Sci Technol 58:881–885

    Article  CAS  Google Scholar 

  10. Chang IS, Jang JK, Gil GC, Kim M, Kim HJ, Cho BW, Kim BH (2004) Continuous determination of biochemical oxygen demand using microbial fuel cell type biosensor. Biosens Bioelectron 19:607–613

    Article  CAS  Google Scholar 

  11. 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 43:7148–7152

    Article  CAS  Google Scholar 

  12. Chae KJ, Choi MF, Kim KY, Ajayi FF, Park W, Kim CH, Kim IS (2010) Methanogenesis control by employing various environmental stress conditions in two-chambered microbial fuel cells. Bioresour Technol 101:5350–5357

    Article  CAS  Google Scholar 

  13. 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:e00103-10

    Google Scholar 

  14. Steinbusch KJ, Hamelers HV, Schaap JD, Kampman C, Buisman CJ (2010) Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. Environ Sci Technol 44:513–517

    Article  CAS  Google Scholar 

  15. 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 41:2554–2559

    Article  CAS  Google Scholar 

  16. Butler CS, Clauwaert P, Green SJ, Verstraete W, Nerenberg R (2010) Bioelectrochemical perchlorate reduction in microbial fuel cell. Environ Sci Technol 44:4685–4691

    Article  CAS  Google Scholar 

  17. ter Hejne A, Liu F, van der Weijden R, Weijma J, Buisman CJN, Hamelers HVM (2010) Copper recovery combined with electricity production in a microbial fuel cell. Environ Sci Technol 44:4376–4381

    Article  CAS  Google Scholar 

  18. Modin O, Wang X, Wu X, Rauch S, Fedje KK (2012) Bioelectrochemical recovery of Cu, Pb, Cd, and Zn from dilute solutions. J Hazard Mater 235:291–297

    Article  CAS  Google Scholar 

  19. Park HI, Kim DK, Choi YJ, Pak D (2005) Nitrate reduction using an electrode as direct electron donor in a biofilm-electrode reactor. Process Biochem 40:3383–3388

    Article  CAS  Google Scholar 

  20. Zhang Y, Angelidaki I (2014) Microbial electrolysis cells turning to be versatile technology: recent advances and future challenges. Water Res 56:11–25

    Article  CAS  Google Scholar 

  21. Liu H, Grot S, Logan BE (2005) Electrochemically assisted microbial production of hydrogen from acetate. Environm Sci Technol 39:4317–4320

    Article  CAS  Google Scholar 

  22. Cheng S, Xing D, Call DF, Logan BE (2009) Direct biological conversion of electrical current into methane by electromethanogenesis. Environ Sci Technol 43:3953–3958

    Article  CAS  Google Scholar 

  23. Rabaey K, Girguis P, Nielsen LK (2011) Metabolic and practical considerations on microbial electrosynthesis. Curr Opin Biotechnol 22:371–377

    Article  CAS  Google Scholar 

  24. Sharma M, Aryal N, Sarma PM, Vanbroekhoven K, Lal B, Benetton XD, Pang D (2013) Bioelectrocalatyzed reduction of acetic and butyric acids via direct electron transfer using a mixed culture of sulfate-reducers drives electrosynthesis of alcohols and acetone. Chem Comm 49:6495–6497

    Article  CAS  Google Scholar 

  25. Heijnen JJ (1999) Bioenergetics of microbial growth. In: Flickinger MC, Drew SD (eds) Encyclopedia of bioprocess technology: fermentation, biocatalysis, and bioseparation. Wiley, New York, pp 267–291

    Google Scholar 

  26. Logan BE, Hamelers B, Rozendal R, Schröder U, Keller J, Fregula S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40:5181–5192

    Article  CAS  Google Scholar 

  27. Rabaey K, Rodríguez J, Blackall LL, Keller J, Gross P, Batstone D, Verstraete W, Nealson KH (2007) Microbial ecology meets electrochemistry: electricity-driven and driving communities. Int Soc Microb Ecol J 1:9–18

    CAS  Google Scholar 

  28. Rismani-Yazdi H, Carver SM, Christy AD, Tuovinen OH (2008) Cathodic limitations in microbial fuel cells: an overview. J Power Sources 180:683–694

    Article  CAS  Google Scholar 

  29. Pham TH, Aelterman P, Verstraete W (2009) Bioanode performance in bioelectrochemical systems: recent improvements and prospects. Trends Biotechnol 27:168–178

    Article  CAS  Google Scholar 

  30. Clauwaert P, Aelterman P, Pham TH, de Schamphelaire L, Carballa M, Rabaey K, Verstraete W (2008) Minimizing losses in bio-electrochemical systems: the road to applications. Appl Microbiol Biotechnol 79:901–913

    Article  CAS  Google Scholar 

  31. Clauwaert P, van der Ha D, Verstraete W (2008) Energy recovery from energy rich vegetable products with microbial fuel cells. Biotechnol Lett 30:1947–1951

    Article  CAS  Google Scholar 

  32. Behera M, Jana PS, More TT, Ghangrekar MM (2010) Rice mill wastewater treatment in microbial fuel cells fabricated using proton exchange membrane and earthen pot at different pH. Bioelectrochem 79:228–233

    Article  CAS  Google Scholar 

  33. Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555

    Article  CAS  Google Scholar 

  34. Zuo Y, Xing D, Regan JM, Logan BE (2008) Isolation of the exoelectrogenic bacterium Ochobactrum anthropic YZ-1 by using a U-tube microbial fuel cell. Appl Environ Microbiol 74:3130–3137

    Article  CAS  Google Scholar 

  35. Ringeisen BR, Henderson E, Wu PK, Pietron J, Ray R, Little B, Biffinger JC, Jones-Meean JM (2006) High power density from a miniature microbial fuel cell using Shewanella oneidensis DSP10. Environ Sci Technol 40:2629–2634

    Article  CAS  Google Scholar 

  36. Chaudhuri SK, Lovley DR (2003) Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nat Biotechnol 21:1229–1232

    Article  CAS  Google Scholar 

  37. Chung K, Okabe S (2009) Characterization of electrochemical activity of a strain ISO2-3 phylogenetically related to Aeromonas sp. isolated from a glucose-fed microbial fuel cell. Biotechnol Bioeng 104:901–910

    Article  CAS  Google Scholar 

  38. Freguia S, Rabaey K, Yuan Z, Keller J (2008) Syntrophic processes drive the conversion of glucose in microbial fuel cell anodes. Environ Sci Technol 42:7937–7943

    Google Scholar 

  39. Miller LG, Oremland RS (2008) Electricity generation by anaerobic bacteria and anoxic sediments from hypersaline soda lakes. Extremophiles 12:837–848

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  42. Borole AP, Reguera G, Ringeisen B, Wang ZW, Feng Y, Kim BH (2011) Electroactive biofilms: current status and future research needs. EnergyEnviron Sci 4:4813–4834

    CAS  Google Scholar 

  43. 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 Technol 30:145–152

    Article  CAS  Google Scholar 

  44. Chae KJ, Choi MJ, Lee JW, Kim KY, Kim IS (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Bioresour Technol 100:3518–3525

    Article  CAS  Google Scholar 

  45. Mäkinen AE, Lay CH, Nissilä ME, Puhakka JA (2013) Bioelectricity production on xylose with a compost enrichment culture. Int J Hydrogen Energy 38:15606–15612

    Article  CAS  Google Scholar 

  46. Zhao F, Rahunen N, Varcoe JR, Roberts AJ, Avignone-Rossa C, Thumser AE, Slade RCT (2009) Factors affecting the performance of microbial fuel cells for sulfur pollutants removal. Biosens Bioelectron 24:1931–1936

    Article  CAS  Google Scholar 

  47. El-Naggar MY, Gorby YA, Xia W, Nealson KH (2008) The molecular density of states in bacterial nanowires. Biophys J 95:L10–L12

    Article  CAS  Google Scholar 

  48. Lovley DR (2011) Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ Sci 4:4896–4906

    Article  CAS  Google Scholar 

  49. Kim BH, Kim HJ, Hyun MS, Park DH (1999) Direct electrode reaction of Fe(III)-reducing bacterium, Shewanella putrefaciens. J Microbiol Biotechnol 9:127–131

    Google Scholar 

  50. Schröder U (2007) Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency. Phys Chem Chem Phys 9:2619–2629

    Article  Google Scholar 

  51. Jiang D, Li B, Jia W, Lei Y (2010) Effect of inoculum types on bacterial adhesion and power production in microbial fuel cells. Appl Biochem Biotechnol 160:182–196

    Article  CAS  Google Scholar 

  52. Sun M, Mu ZX, Chen YP, Cheng GP, Liu XW, Chen YZ, Zhao Y, Wang HL, Yu HQ, Wei L, Ma F (2009) Microbe-assisted sulfide oxidation in the anode of a microbial fuel cell. Environ Sci Technol 43:3372–3377

    Article  CAS  Google Scholar 

  53. Catal T, Li K, Bermek H, Liu H (2008) Electricity production from twelve monosaccharides using microbial fuel cells. JPower Sources 175:196–200

    Article  CAS  Google Scholar 

  54. Angenent LT, Karim K, Al-Dahhan MH, Wrenn BA, Domíguez-Espinosa R (2004) Production of bioenergy and biochemicals from industrial and agricultural wastewater. Trends Biotechnol 22:477–485

    Article  CAS  Google Scholar 

  55. Chang IS, Moon H, Bretschger O, Jang JK, Park HI, Nealson KH, Kim BH (2006) Electrochemically active bacteria (EAB) and mediator-less microbial fuel cells. J Microbiol Biotechnol 16:163–177

    CAS  Google Scholar 

  56. Du Z, Li H, Gu T (2007) A state of the art review on microbial fuel cells: a promising technology for wastewater treatment and bioenergy. Biotechnol Adv 25:464–482

    Google Scholar 

  57. Han JL, Wang CT, Hu YC, Liu Y, Chen WM, Chang CT, Xu HZ, Chen BY (2010) Exploring power generation of single-chamber microbial fuel cell using mixed and pure cultures. J Taiwan Inst Chem Eng 41:606–611

    Article  CAS  Google Scholar 

  58. Holmes DE, Bond DR, Lovley DR (2004) Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl Environ Microbiol 70:1234–1237

    Article  CAS  Google Scholar 

  59. Xing D, Cheng S, Logan BE, Regan JM (2010) Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Appl Microbiol Biotechnol 85:1575–1587

    Article  CAS  Google Scholar 

  60. Pham TH, Rabaey K, Aelterman P, Cauwaert P, de Schamphelaire L, Boon N, Verstraete W (2006) Microbial fuel cells in relation to conventional anaerobic digestion technology. Eng Life Sci 6:285–292

    Article  CAS  Google Scholar 

  61. Park HS, Kim BH, Kim HS, Kim HJ, Kim TG, 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 7:297–306

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  63. Rezaei F, Xing D, Wagner R, Regan JM, Richard TL, Logan BE (2009) Simultaneous cellulose degradation and electricity production by Enterobacter cloacae in a microbial fuel cell. Appl Environ Microbiol 75:3673–3678

    Article  CAS  Google Scholar 

  64. 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 8:1805–1815

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  66. Bond DR, Lovley DR (2005) Evidence for involvement of an electron shuttle in electricity generation by Geothrix fermentans. Appl Environ Microbiol 71:2186–2189

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  68. Abrevaya XC, Sacco N, Mauas PJD, Cortón E (2011) Archaea-based microbial fuel cell operating at high ionic strength conditions. Extremophiles 15:633–642

    Article  CAS  Google Scholar 

  69. Zhang L, Zhou S, Zhuang L, Li W, Zhang J, Lu N, Deng L (2008) Microbial fuel cell based on Klebsiella pneuoniae biofilm. Electrochem Comm 10:1641–1643

    Article  CAS  Google Scholar 

  70. 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 76:14–18

    Article  CAS  Google Scholar 

  71. Pham TH, 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 a Gram-positive bacterium to achieve extracellular electron transfer. Appl Microbiol Biotechnol 77:1119–1129

    Article  CAS  Google Scholar 

  72. Liu ZD, Li HR (2007) Effects of bio- and abio-factors on electricity production in a mediatorless microbial fuel cell. Biochem Eng J 36:209–214

    Article  CAS  Google Scholar 

  73. Xing D, Zuo Y, Cheng S, Regan JM, Logan BE (2008) Electricity generation by Rhodopseudomonas palustris DX-1. Environ Sci Technol 42:4146–4151

    Article  CAS  Google Scholar 

  74. 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. Bioresour Technol 102:290–297

    Article  CAS  Google Scholar 

  75. Huang J, Sun B, Zhang X (2010) Electricity generation at high ionic strength in microbial fuel cell by a newly isolated Shewanella marisflavi EP1. Appl Microbiol Biotechnol 85:1141–1149

    Article  CAS  Google Scholar 

  76. Gorby YA, Yanina S, McLeanJS RKM, 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 nanowire by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci U S A 103:11358–11363

    Article  CAS  Google Scholar 

  77. 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 cell. ISME J 2:1146–1156

    Google Scholar 

  78. Marshall CW, May HD (2009) Electrochemical evidence of direct electrode reduction by a thermophilic Gram-positive bacterium, Thermincola ferriacetica. Energy Environ Sci 2:699–705

    Article  CAS  Google Scholar 

  79. Choi Y, Jung E, Park H, Paik SR, Jung S, Kim S (2004) Construction of microbial fuel cells using thermophilic microorganisms, Bacillus licheniformis and Bacillus thermoglucosidasius. Bull Korean Chem Soc 25:813–818

    Article  CAS  Google Scholar 

  80. Oh SE, Logan BE (2005) Hydrogen and electricity production from a food processing wastewater using fermentation and microbial fuel cell technologies. Water Res 39:4673–4682

    Article  CAS  Google Scholar 

  81. You S, Zhao Q, Zhang J, Jiang J, Zhao S (2006) A microbial fuel cell using permanganate as the cathodic electron acceptor. J Power Sources 162:1409–1415

    Google Scholar 

  82. Jong BC, Kim BH, Chang IS, Liew PWY, Choo YF, Kang GS (2006) Enrichment performance, and microbial diversity of a thermophilic mediatorless microbial fuel cell. Environ Sci Technol 40:6449–6454

    Article  CAS  Google Scholar 

  83. Liu H, Logan BE (2004) Electricity generation using an air-cathode single chamber microbial fuel cell in the presence and absence of a proton exchange membrane. Environ Sci Technol 38:4040–4046

    Article  CAS  Google Scholar 

  84. Zhang Y, Min B, Huang L, Angelidaki I (2011) Electricity generation and microbial community response to substrate changes in microbial fuel cell. Bioresour Technol 102:1166–1173

    Article  CAS  Google Scholar 

  85. Huang L, Logan BE (2008) Electricity generation and treatment of paper recycling wastewater using a microbial fuel cell. Appl Microbiol Biotechnol 80:349–355

    Article  CAS  Google Scholar 

  86. Carver SM, Vuoriranta P, Tuovinen OH (2011) A thermophilic microbial fuel cell design. J Power Sources 196:3757–3370

    Google Scholar 

  87. Nercessian O, Parot S, Délia ML, Bergel A, Achouak W (2012) Harvesting electricity with Geobacter bremensis isolated from compost. PLoS One 7:1–8

    Article  CAS  Google Scholar 

  88. Rismani-Yazdi H, Christy AD, Dehority BA, Morrison M, Yu Z, Tuovinen OH (2007) Electricity generation from cellulose by rumen microorganisms in microbial fuel cells. Biotechnol Bioeng 97:1398–1407

    Article  CAS  Google Scholar 

  89. Ishii S, Shimoyama T, Hotta Y, Watanabe K (2008) Characterization of a filamentous biofilm community established in a cellulose-fed microbial fuel cell. BMC Microbiol 8:6

    Google Scholar 

  90. Mathis BJ, Marshall CW, Milliken CE, Makkar RS, Creager SE, May HD (2008) Electricity generation by thermophilic microorganisms from marine sediment. Appl Microbiol Biotechnol 78:147–155

    Article  CAS  Google Scholar 

  91. Phung NT, Lee J, Kang KH, Chang IS, Gadd GM, Kim BH (2004) Analysis of microbial diversity in oligotrophic microbial fuel cells using 16S rRNA sequences. FEMS Microbiol Lett 223:77–82

    Article  CAS  Google Scholar 

  92. Zhu H, Béland M (2006) Evaluation of alternative methods of preparing hydrogen producing seeds from digested wastewater sludge. Int J Hydrogen Energy 31:1980–1988

    Article  CAS  Google Scholar 

  93. He Z, Shelley D, Minteer SD, Angenent LT (2005) Electricity generation from artificial wastewater using an upflow microbial fuel cell. Environ Sci Technol 39:5262–5267

    Article  CAS  Google Scholar 

  94. Rismani-Yazdi H, Carver SM, Christya AD, Yu Z, Bibby K, Peccia J, Tuovinen OH (2013) Suppression of methanogenesis in cellulose-fed microbial fuel cells in relation to performance, metabolite formation, and microbial population. Bioresour Technol 129:281–288

    Article  CAS  Google Scholar 

  95. Chung K, Okabe S (2009) Continuous power generation and microbial community structure of the anode biofilms in a three-stage microbial fuel cell system. Appl Microbiol Biotechnol 83:965–977

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  97. Cheng S, Kiely P, Logan BE (2011) Pre-acclimation of a wastewater inoculum to cellulose in an aqueous-cathode MEC improves power generation in air-cathode MFCs. Bioresour Technol 102:367–371

    Article  CAS  Google Scholar 

  98. Lovley DR (2008) The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 19:564–571

    Article  CAS  Google Scholar 

  99. Geelhoed JS, Hamelers HVM, Stams AJM (2010) Electricity-mediated biological hydrogen production. Curr Opin Microbiol 13:307–315

    Article  CAS  Google Scholar 

  100. 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 71:4414–4426

    Article  CAS  Google Scholar 

  101. Reguera G, Pollina RB, Nicoll JS, Lovley DR (2007) Possible nonconductive role of Geobacter sulfurreducens pilus nanowires in biofilm formation. J Bacteriol 189:2125–2127

    Article  CAS  Google Scholar 

  102. 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 105:3968–3973

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  105. Stams AJ, de Bok FA, Plugge CM, van Eekert MH, Dolfing J, Schraa G (2006) Exocellular electron transfer in anaerobic microbial communities. Environ Microbiol 8:371–382

    Article  CAS  Google Scholar 

  106. Gil GC, Chang IS, Kim BH, Kim M, Jang JK, Park HS, Kim HJ (2003) Operational parameters affecting the performance of a mediator-less microbial fuel cell. Biosens Bioelectr 18:327–334

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  108. Childers SE, Ciufo S, Lovley DR (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416:767–769

    Article  CAS  Google Scholar 

  109. Aelterman P, Rabaey K, Pham HT, Boom N, Verstraete W (2006) Continuous electricity generation at high voltages and currents using stacked microbial fuel cells. Environ Sci Technol 40:3388–3394

    Article  CAS  Google Scholar 

  110. Bretschger O, Obraztsove 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 73:7003–7012

    Article  CAS  Google Scholar 

  111. 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 Acta 73:5292–5307

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  113. Coma M, Puig S, Pous N, Balaguer MD, Colprim J (2013) Biocatalysis sulphate removal in a BES cathode. Bioresour Technol 130:218–223

    Article  CAS  Google Scholar 

  114. 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 Sci 65:2912–2917

    CAS  Google Scholar 

  115. Foley JM, Rozendal RA, Hertle CK, Lant PA, Rabaey K (2010) Life cycle assessment of high-rate anaerobic treatment, microbial fuel cells, and microbial electrolysis cells. Environ Sci Technol 44:3629–3637

    Article  CAS  Google Scholar 

  116. Dumas C, Basseguy R, Bergel A (2008) Microbial electrocatalysis with Geobacter sulfurreducens biofilm on stainless stell cathodes. Electrochim Acta 53:2494–2500

    Article  CAS  Google Scholar 

  117. Gregory KB, Bond DR, Lovley DR (2004) Graphite electrode as electron donors for anaerobic respiration. Environ Microbiol 6:596–604

    Article  CAS  Google Scholar 

  118. 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 181:2403–2410

    CAS  Google Scholar 

  119. Thrash JC, van Trump JI, Wever KA, Miller E, Achenbach LA, Coates JD (2007) Electrochemical stimulation of microbial perchlorate reduction. Environ Sci Technol 41:1740–1746

    Article  CAS  Google Scholar 

  120. 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. Electroanalysis 14:913–922

    Article  CAS  Google Scholar 

  121. 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 tetrachloroethene by Geobacter lovleyi. Appl Environ Microbiol 74:5943–5947

    Google Scholar 

  122. Gregory KB, Lovley DR (2005) Remediation and recovery of uranium from contaminated subsurface environments with electrodes. Environ Sci Technol 39:8943–8947

    Article  CAS  Google Scholar 

  123. Zhang LH, Jia JP, Ying DW, Zhu NW, Zhu YC (2005) Electrochemical effect on denitrification in different microenvironments around anodes and cathodes. Res Microbiol 156:88–92

    Article  CAS  Google Scholar 

  124. Jeremiasse AW, Hamelers HVM, Buisman CJN (2010) Microbial electrolysis cell with a microbial biocathode. Bioelectrochemistry 78:39–43

    Article  CAS  Google Scholar 

  125. 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. Bioresour Technol 101:3085–3090

    Article  CAS  Google Scholar 

  126. 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 ethane. Biosens Bioelectron 25:1796–1802

    Article  CAS  Google Scholar 

  127. Tandukar M, Huber SJ, Onodera T, Pavlostathis SG (2009) Biological chromium(VI) reduction in the cathode of a microbial fuel cell. Environ Sci Technol 43:8159–8165

    Article  CAS  Google Scholar 

  128. Croese E, Pereira MA, Euverink GJW, Stams AJM, Geeldhoed JS (2011) Analysis of the microbial community of the biocathode of a hydrogen-producing microbial electrolysis cell. Appl MicrobiolBiotechnol 92:1083–1093

    CAS  Google Scholar 

  129. Logan BE, Call D, Cheng S, Hamelers HVM, Sleitels THJA, Jeremiasse AW, Rozendal RA (2008) Microbial electrolysis cells for high yield hydrogen gas production from organic matter. Environ Sci Technol 42:8630–8640

    Article  CAS  Google Scholar 

  130. Wang A, Liu W, Cheng S, Xing D, Zhou J, Logan BE (2009) Source of methane and methods to control its formation in single chamber microbial electrolysis cells. Int J Hydrogen Energy 34:3653–3658

    Article  CAS  Google Scholar 

  131. Strychartz SM, Glaven R, Coppi M, Gannon S, Perpetua L, Liu A, Nevin K, Lovley DR (2011) Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemicstry 80:142–150

    Article  CAS  Google Scholar 

  132. van Groenestijn JW, Hazewinkel JHO, Nienoord M, Bussmann BJT (2002) Energy aspects of biological hydrogen production in high rate bioreactors operated in the thermophilic temperature range. Int J Hydrogen Energy 27:1141–1147

    Article  Google Scholar 

  133. Zumdahl SS (1998) Chemical principles, 3rd edn. Hourson Mifflin Company, Boston, 1040 pp

    Google Scholar 

  134. Min B, Román ÓB, Angelidaki I (2008) Importance of temperature and anodic medium composition on microbial fuel cell (MFC) performance. Biotechnol Lett 30:1213–1218

    Article  CAS  Google Scholar 

  135. 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 26:803–808

    Article  CAS  Google Scholar 

  136. Hallenbeck PC (2005) Fundamentals of fermentative production of hydrogen. Water Sci Technol 52:21–29

    CAS  Google Scholar 

  137. Borole AP, Hamilton CY, Vishnivetskaya T, Leak D, Andras C (2009) Improving power production in acetate-fed microbial fuel cells via enrichment of exoelectrogenic organisms in flow-through systems. Biochem Eng J 48:71–80

    Article  CAS  Google Scholar 

  138. Biffinger JC, Pietron J, Bretschger O, Nadeau LJ, Johnson GR, Williams CC, Nealson KH, Ringeisen BR (2008) The influence of acidity on microbial fuel cells containing Shewanella oneidensis. Biosens Bioelectron 24:900–905

    Article  CAS  Google Scholar 

  139. Borole AP, O’Neill H, Tsouris C, Cesar S (2008) A microbial fuel cell operating at low pH using the acidophile Acidiphilium cryptum. Biotechnol Lett 30:1367–1372

    Google Scholar 

  140. Sulonen ML, Kokko ME, Lakaniemi AM, Puhakka JA (2015) Electricity generation from tetrathionate in microbial fuel cells by acidophiles. J Hazard Mater 284:182–189

    Article  CAS  Google Scholar 

  141. Franks AE, Nevin KP, Jia H, Izallalen M, Woodard TL, Lovley DR (2009) Novel strategy for three-dimensional real-time imaging of microbial fuel cell communities: monitoring the inhibitory effects of proton accumulation within the anode biofilm. Energy Environ Sci 2:113–119

    Article  CAS  Google Scholar 

  142. Torres CI, Marcus AK, Rittmann BE (2008) Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria. Biotechnol Bioeng 100:872–881

    Article  CAS  Google Scholar 

  143. Ren Z, Ward TE, Regan JM (2007) Electricity production from cellulose in a microbial fuel cell using a defined binary culture. Environ Sci Technol 41:4781–4786

    Article  CAS  Google Scholar 

  144. Wang X, Feng YJ, Lee H (2008) Electricity production from beer brewery wastewater using single chamber microbial fuel cell. Water Sci Technol 57:1117–1121

    Article  CAS  Google Scholar 

  145. Rodrigo MA, Cañizares P, Carcía H, Linares JJ, Lobato J (2009) Study of the acclimation stage and of the effect of the biodegradability on the performance of a microbial fuel cell. Bioresour Technol 100:4704–4710

    Article  CAS  Google Scholar 

  146. Velasquez-Orta SB, Yu E, Katuri KP, Head IM, Curtis TP, Scott K (2011) Evaluation of hydrolysis and fermentation rates in microbial fuel cells. Appl Microbiol Biotechnol 90:789–798

    Article  CAS  Google Scholar 

  147. Lee HS, Parameswaran P, Kato-Marcus A, Torres CI, Rittmann BE (2008) Evaluation of energy-conversion efficiencies in microbial fuel cells (MFCs) utilizing fermentable and non-fermentable substrates. Water Res 42:1501–1510

    Article  CAS  Google Scholar 

  148. Nam JY, Kim HW, Lim KH, Shin HS (2010) Effects of organic loading rates on the continuous electricity generation from fermented wastewater using a single-chamber microbial fuel cell. Bioresour Technol 101:S33–S37

    Article  CAS  Google Scholar 

  149. Torres CI, Marcus AK, Rittmann BE (2007) Kinetics of consumption of fermentation products by anode-respiring bacteria. Appl Microbiol Biotechnol 77:689–697

    Article  CAS  Google Scholar 

  150. Behera M, Ghangrekar MM (2009) Performance of microbial fuel cell in response to change in sludge loading rate at different anodic feed pH. Bioresour Technol 100:5114–5121

    Article  CAS  Google Scholar 

  151. Aelterman P, Versichele M, Marzorati M, Boon V, Verstraete W (2008) Loading rate and external resistance control the electricity generation in microbial fuel cells with different three-dimensional anodes. Bioresour Technol 99:8895–8902

    Article  CAS  Google Scholar 

  152. Sharma Y, Li B (2010) The variation of power generation with organic substrates in single-chamber microbial fuel cells (SCMFCs). Bioresour Technol 101:1844–1850

    Article  CAS  Google Scholar 

  153. Sleutels THJA, Hamelers HVM, Buisman CJN (2011) Effect of mass and charge transport speed and direction in porous anodes on microbial electrolysis cell performance. Bioresour Technol 102:399–403

    Article  CAS  Google Scholar 

  154. Lee HS, Torres CI, Rittmann BE (2009) Effects of substrate diffusion and anode potential on kinetic parameters for anode-respiring bacteria. Environ Sci Technol 43:7571–7577

    Article  CAS  Google Scholar 

  155. Mohan SV, Raghavulu SV, Srikanth S, Sarma PN (2007) Bioelectricity production by mediatorless microbial fuel cell under acidophilic condition using wastewater as substrate: influence of substrate loading rate. Curr Sci 92:1720–1726

    CAS  Google Scholar 

  156. Martin E, Savadogo O, Guiot SR, Tartakovsky B (2010) The influence of operational conditions on the performance of a microbial fuel cell seeded with mesophilic anaerobic sludge. Biochem Eng J 51:132–139

    Article  CAS  Google Scholar 

  157. Liu H, Cheng S, Logan BE (2005) Production of electricity from acetate or butyrate using a single-chamber microbial fuel cell. Environ Sci Technol 39:658–662

    Article  CAS  Google Scholar 

  158. Jung S, Regan JM (2011) Influence of external resistance on electrogenesis, methanogenesis, and anode prokaryotic communities in microbial fuel cells. Appl Environ Microbiol 77:564–571

    Article  CAS  Google Scholar 

  159. Aelterman P, Freguia S, Keller J, Verstraete W, Rabaey K (2008) The anode potential regulates bacterial activity in microbial fuel cells. Appl Microbiol Technol 78:409–418

    Article  CAS  Google Scholar 

  160. Rismani-Yazdi H, Christy AD, Carver SM, Yu Z, Dehority BA, Tuovinen OH (2011) Effect of external resistance on bacterial diversity and metabolism in cellulose-fed microbial fuel cells. Bioresour Technol 102:278–283

    Article  CAS  Google Scholar 

  161. Lefebvre O, Shen Y, Tan Z, Uzabiaga A, Chang IS, Ng HY (2011) A comparison of membranes and enrichment strategies for microbial fuel cells. Bioresour Technol 102:6291–6294

    Article  CAS  Google Scholar 

  162. Bond DR (2010) Electrodes as electron acceptors, and the bacteria who love them. In: Barton LL, Mandl M, Loy A (eds) Geomicrobiology: molecular and environmental perspective. Springer, Netherlands, pp 385–399

    Google Scholar 

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

    Article  CAS  Google Scholar 

  164. Wagner RC, Call DF, Logan BE (2010) Optimal set anode potentials vary in bioelectrochemical systems. Environ Sci Technol 44:6036–6041

    Article  CAS  Google Scholar 

  165. Wei J, Liang P, Cao X, Huang W (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 44:3187–3191

    Article  CAS  Google Scholar 

  166. Torres CI, Krajmalnik-Brown R, Parameswaran P, Kato Marcus A, Wanger G, Gorby YA, Rittmann BE (2009) Selecting anode-respiring bacteria based on anode potential: phylogenetic, electrochemical and microscopic characterization. Environ Sci Technol 43:9519–9524

    Article  CAS  Google Scholar 

  167. Sun D, Call DF, Kiely PD, Wang A, Logan BE (2012) Syntrophic interactions improve power production in formic acid fed MFCs operated with set anode potentials or fixed resistances. Biotechnol Bioeng 109:405–414

    Article  CAS  Google Scholar 

  168. Li F, Sharma Y, Lei Y, Li B, Zhou Q (2010) Microbial fuel cells: the effects of configurations, electrolyte solutions, and electrode materials on power generation. Appl Biochem Biotechnol 160:168–181

    Article  CAS  Google Scholar 

  169. Liu Y, Harnisch F, Fricke K, Schröder U, Climent V, Feliu JM (2010) The study of electrochemically active microbial biofilms on different carbon-based anode materials in microbial fuel cells. Biosens Bioelectron 25:2167–2171

    Article  CAS  Google Scholar 

  170. Logan BE (2010) Scaling up microbial fuel cells and other bioelectrochemical systems. Appl Microbiol Biotechnol 85:1665–1671

    Article  CAS  Google Scholar 

  171. Logan B, Cheng S, Watson V, Estadt G (2007) Graphite fiber brush anodes for increased power production in air-cathode microbial fuel cells. Environ Sci Technol 41:3341–3346

    Article  CAS  Google Scholar 

  172. Mohanakrishna G, Mohan SK, Mohan SV (2012) Carbon based nanotubes and nanopowder as impregnated electrode structures for enhanced power generation: evaluation with real field wastewater. Appl Energy 95:31–37

    Article  CAS  Google Scholar 

  173. Wei J, Liang P, Huang X (2011) Recent progress in electrodes for microbial fuel cells. Bioresour Technol 102:9335–9344

    Article  CAS  Google Scholar 

  174. Gnana Kumar G, Sathiya Sarathi VG, Nahm KS (2013) Recent advances and challenges in the anode architecture and their modification for the applications of microbial fuel cells. Biosens Bioelectron 43:461–475

    Article  CAS  Google Scholar 

  175. Zhang X, Cheng S, Wang X, Huang X, Logan BE (2009) Separator characteristics for increasing performance of microbial fuel cells. Environ Sci Technol 43:8456–8461

    Article  CAS  Google Scholar 

  176. Jia YH, Tran HT, Kim DH, Oh SJ, Park DH, Zhang RH, Ahn DH (2008) Simultaneous organics removal and bio-electrochemical denitrification in microbial fuel cells. Bioprocess Biosyst Eng 31:315–321

    Article  CAS  Google Scholar 

  177. Lovley DR, Nevin KP (2011) A shift in the current: new applications and concepts for microbe-electrode electron exchange. Curr Opin Biotechnol 22:441–448

    Article  CAS  Google Scholar 

  178. Jiang D, Curtis M, Troop E, Scheible K, McGrath J, Hu B, Suib S, Raymond D, Li B (2011) A pilot-scale study on utilizing multi-anode/cathode microbial fuel cells (MAC MFCs) to enhance the power production in wastewater treatment. Int J Hydrogen Energy 36:876–884

    Article  CAS  Google Scholar 

  179. Cusick RD, Bryan B, Parker DS, Merrill MD, Mehanna M, Kiely PD, Liu G, Logan BE (2011) Performance of a pilot-scale continuous flow microbial electrolysis cell. Appl Microbiol Biotechnol 89:2053–2063

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry and Bioengineering, Tampere University of Technology, Tampere, Finland

    Marika E. Kokko, Annukka E. Mäkinen & Jaakko A. Puhakka

Authors
  1. Marika E. Kokko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Annukka E. Mäkinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaakko A. Puhakka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marika E. Kokko .

Editor information

Editors and Affiliations

  1. Biotechnology, Department of Chemistry Center for Chemistry & Chemical Engineering, Lund University, Lund, Sweden

    Rajni Hatti-Kaul

  2. Biotechnology, Department of Chemistry Center for Chemistry & Chemical Engineering, Lund University, Lund, Sweden

    Gashaw Mamo

  3. Biotechnology, Department of Chemistry Center for Chemistry & Chemical Engineering, Lund University, Lund, Sweden

    Bo Mattiasson

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kokko, M.E., Mäkinen, A.E., Puhakka, J.A. (2016). Anaerobes in Bioelectrochemical Systems. In: Hatti-Kaul, R., Mamo, G., Mattiasson, B. (eds) Anaerobes in Biotechnology. Advances in Biochemical Engineering/Biotechnology, vol 156. Springer, Cham. https://doi.org/10.1007/10_2015_5001

Download citation

Publish with us

Policies and ethics

Search

Navigation