Redox Interactions of Organohalide-Respiring Bacteria (OHRB) with Solid-State Electrodes: Principles and Perspectives of Microbial Electrochemical Remediation

  • Federico AulentaEmail author
  • Simona Rossetti
  • Bruna Matturro
  • Valter Tandoi
  • Roberta Verdini
  • Mauro Majone


Recent studies have revealed that a number of organohalide-respiring bacteria (OHRB) are capable to establish redox interactions with solid-state electrodes by using them as direct or indirect electron donors in their energy metabolism. Although the biochemical, ecological, and evolutionary significance of electron transfer capabilities in OHRB remain largely unknown, they are increasingly being considered for bioremediation applications. In principle, bioelectrochemical remediation systems which use insoluble electrodes to drive the microbial reduction of chlorinated compounds offer numerous advantages compared to conventional approaches, such as the possibility to fine-tune the rate of electron delivery and consumption, avoid injection of chemicals to the subsurface environment and ultimately gain a more direct control over the biodegradation reactions taking place at the electrodes. In spite of that, however, the technology is still in its infancy and further research and extensive field testing is needed to prove its actual potential for site remediation.


Methyl Viologen Cathode Potential Redox Mediator Direct Electron Transfer Standard Hydrogen Electrode 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

List of Abbreviations




Bioelectrochemical systems




Direct electron transfer


Direct interspecies electron transfer


Extracellular electron transfer




Methyl viologen


Organohalide-respiring bacteria




Standard hydrogen electrode




Vinyl chloride


  1. Aulenta F, Gossett JM, Papini MP, Rossetti S, Majone M (2005) Comparative study of methanol, butyrate, and hydrogen as electron donors for long-term dechlorination of tetrachloroethene in mixed anerobic cultures. Biotechnol Bioeng 91(6):743–753CrossRefPubMedGoogle Scholar
  2. Aulenta F, Catervi A, Majone M, Panero S, Reale P, Rossetti S (2007a) Electron transfer from a solid-state electrode assisted by methyl viologen sustains efficient microbial reductive dechlorination of TCE. Environ Sci Technol 41(7):2554–2559. doi: 10.1021/es0624321 CrossRefPubMedGoogle Scholar
  3. Aulenta F, Pera A, Rossetti S, Papini MP, Majone M (2007b) Relevance of side reactions in anaerobic reductive dechlorination microcosms amended with different electron donors. Water Res 41(1):27–38CrossRefPubMedGoogle Scholar
  4. Aulenta F, Canosa A, Majone M, Panero S, Reale P, Rossetti S (2008a) 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(16):6185–6190CrossRefPubMedGoogle Scholar
  5. Aulenta F, Reale P, Catervi A, Panero S, Majone M (2008b) Kinetics of trichloroethene dechlorination and methane formation by a mixed anaerobic culture in a bio-electrochemical system. Electrochim Acta 53(16):5300–5305CrossRefGoogle Scholar
  6. 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(1):85–91CrossRefPubMedGoogle Scholar
  7. Aulenta F, Di Maio V, Ferri T, Majone M (2010) The humic acid analogue antraquinone-2,6-disulfonate (AQDS) serves as an electron shuttle in the electricity-driven microbial dechlorination of trichloroethene to cis-dichloroethene. Bioresour Technol 101(24):9728–9733CrossRefPubMedGoogle Scholar
  8. Aulenta F, Ferri T, Nicastro D, Majone M, Papini MP (2011a) Improved electrical wiring of microbes: anthraquinone-modified electrodes for biosensing of chlorinated hydrocarbons. New Biotechnol 29(1):126–131CrossRefGoogle Scholar
  9. Aulenta F, Tocca L, Verdini R, Reale P, Majone M (2011b) Dechlorination of trichloroethene in a continuous-flow bioelectrochemical reactor: effect of cathode potential on rate, selectivity, and electron transfer mechanisms. Environ Sci Technol 45(19):8444–8451CrossRefPubMedGoogle Scholar
  10. Aulenta F, Rossetti S, Amalfitano S, Majone M, Tandoi V (2013) Conductive magnetite nanoparticles accelerate the microbial reductive dechlorination of trichloroethene by promoting interspecies electron transfer processes. Chemsuschem 6(3):433–436CrossRefPubMedGoogle Scholar
  11. Aulenta F, Fazi S, Majone M, Rossetti S (2014) Electrically conductive magnetite particles enhance the kinetics and steer the composition of anaerobic TCE-dechlorinating cultures. Process Biochem. doi: 10.1016/j.procbio.2014.09.015 Google Scholar
  12. Cervantes FJ, Martinez CM, Gonzalez-Estrella J, Marquez A, Arriaga S (2013) Kinetics during the redox biotransformation of pollutants mediated by immobilized and soluble humic acids. Appl Microbiol Biotechnol 97(6):2671–2679CrossRefPubMedGoogle Scholar
  13. Chun CL, Payne RB, Sowers KR, May HD (2013) Electrical stimulation of microbial PCB degradation in sediment. Water Res 47(1):141–152CrossRefPubMedGoogle Scholar
  14. Di Battista A, Verdini R, Rossetti S, Pietrangeli B, Majone M, Aulenta F (2012) CARD-FISH analysis of a TCE-dechlorinating biocathode operated at different set potentials. New Biotechnol 30(1):33–38CrossRefGoogle Scholar
  15. Fennell DE, Stover MA, Zinder SH, Gossett JM (1995) Comparison of alternative electron donors to sustain PCE anaerobic reductive dechlorination. Bioremediat Chlorinated Solvents 3(4):9–16Google Scholar
  16. Friedman ES, Rosenbaum MA, Lee AW, Lipson DA, Land BR, Angenent LT (2012) A cost-effective and field-ready potentiostat that poises subsurface electrodes to monitor bacterial respiration. Biosens Bioelectron 32(1):309–313CrossRefPubMedGoogle Scholar
  17. Harnisch F, Aulenta F, Schroeder U (2011) Microbial fuel cells and bioelectrochemical systems: industrial and environmental biotechnologies based on extracellular electron transfer. In: Moo-Young M (ed) Comprehensive biotechnology, 2nd edn. Academic Press, Burlington, pp 643–659CrossRefGoogle Scholar
  18. Ho SV, Sheridan PW, Athmer CJ, Heitkamp MA, Brackin JM, Weber D, Brodsky PH (1995) Integrated in-situ soil remediation technology—the lasagna process. Environ Sci Technol 29(10):2528–2534CrossRefPubMedGoogle Scholar
  19. Ho SV, Athmer C, Sheridan PW, Hughes BM, Orth R, McKenzie D, Brodsky PH, Shapiro A, Thornton R, Salvo J, Schultz D, Landis R, Griffith R, Shoemaker S (1999a) The lasagna technology for in situ soil remediation. 1. Small field test. Environ Sci Technol 33(7):1086–1091CrossRefGoogle Scholar
  20. Ho SV, Athmer C, Sheridan PW, Hughes BM, Orth R, McKenzie D, Brodsky PH, Shapiro AM, Sivavec TM, Salvo J, Schultz D, Landis R, Griffith R, Shoemaker S (1999b) The lasagna technology for in situ soil remediation. 2. Large field test. Environ Sci Technol 33(7):1092–1099CrossRefGoogle Scholar
  21. Huang LP, Regan JM, Quan X (2011) Electron transfer mechanisms, new applications, and performance of biocathode microbial fuel cells. Bioresour Technol 102(1):316–323CrossRefPubMedGoogle Scholar
  22. Huang LP, Chai XL, Quan X, Logan BE, Chen GH (2012) Reductive dechlorination and mineralization of pentachlorophenol in biocathode microbial fuel cells. Bioresour Technol 111:167–174CrossRefPubMedGoogle Scholar
  23. Kassenga GR, Pardue JH (2006) Effect of competitive terminal electron acceptor processes on dechlorination of cis-1,2-dichloroethene and 1,2-dichloroethane in constructed wetland soils. FEMS Microbiol Ecol 57(2):311–323CrossRefPubMedGoogle Scholar
  24. Kong FY, Wang AJ, Ren HY (2014) Improved 4-chlorophenol dechlorination at biocathode in bioelectrochemical system using optimized modular cathode design with composite stainless steel and carbon-based materials. Bioresour Technol 166:252–258CrossRefPubMedGoogle Scholar
  25. Liu D, Lei LC, Yang B, Yu QN, Li ZJ (2013) Direct electron transfer from electrode to electrochemically active bacteria in a bioelectrochemical dechlorination system. Bioresour Technol 148:9–14CrossRefPubMedGoogle Scholar
  26. Löffler FE, Tiedje JM, Sanford RA (1999) Fraction of electrons consumed in electron acceptor reduction and hydrogen thresholds as indicators of halorespiratory physiology. Appl Environ Microbiol 65(9):4049–4056PubMedPubMedCentralGoogle Scholar
  27. Lohner ST, Becker D, Mangold KM, Tiehm A (2011) Sequential reductive and oxidative biodegradation of chloroethenes stimulated in a coupled bioelectro-process. Environ Sci Technol 45(15):6491–6497CrossRefPubMedGoogle Scholar
  28. Lovley DR (2008) Extracellular electron transfer: wires, capacitors, iron lungs, and more. Geobiology 6(3):225–231CrossRefPubMedGoogle Scholar
  29. Lovley DR (2011) Reach out and touch someone: potential impact of DIET (direct interspecies energy transfer) on anaerobic biogeochemistry, bioremediation, and bioenergy. Rev Environ Sci Bio-Technol 10(2):101–105CrossRefGoogle Scholar
  30. Luijten MLGC, Roelofsen W, Langenhoff AAM, Schraa G, Stams AJM (2004a) Hydrogen threshold concentrations in pure cultures of halorespiring bacteria and at a site polluted with chlorinated ethenes. Environ Microbiol 6(6):646–650CrossRefPubMedGoogle Scholar
  31. Luijten MLGC, Weelink SAB, Godschalk B, Langenhoff AAM, van Eekert MHA, Schraa G, Stams AJM (2004b) Anaerobic reduction and oxidation of quinone moieties and the reduction of oxidized metals by halorespiring and related organisms. FEMS Microbiol Ecol 49(1):145–150CrossRefPubMedGoogle Scholar
  32. 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):e00159-11CrossRefPubMedPubMedCentralGoogle Scholar
  33. Morris RM, Sowell S, Barofsky D, Zinder S, Richardson R (2006) Transcription and mass-spectroscopic proteomic studies of electron transport oxidoreductases in Dehalococcoides ethenogenes. Environ Microbiol 8(9):1499–1509. doi: 10.1111/j.1462-2920.2006.01090.x CrossRefPubMedGoogle Scholar
  34. Nijenhuis I, Zinder SH (2005) Characterization of hydrogenase and reductive dehalogenase activities of Dehalococcoides ethenogenes strain 195. Appl Environ Microbiol 71(3):1664–1667CrossRefPubMedPubMedCentralGoogle Scholar
  35. Pous N, Puig S, Coma M, Balaguer MD, Colprim J (2013) Bioremediation of nitrate-polluted groundwater in a microbial fuel cell. J Chem Technol Biotechnol 88(9):1690–1696CrossRefGoogle Scholar
  36. 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(1):324–333CrossRefPubMedGoogle Scholar
  37. Rozendal RA, Hamelers HVM, Rabaey K, Keller J, Buisman CJN (2008) Towards practical implementation of bioelectrochemical wastewater treatment. Trends Biotechnol 26(8):450–459CrossRefPubMedGoogle Scholar
  38. Skadberg B, Geoly-Horn SL, Sangamalli V, Flora JRV (1999) Influence of pH, current and copper on the biological dechlorination of 2,6-dichlorophenol in an electrochemical cell. Water Res 33(9):1997–2010CrossRefGoogle Scholar
  39. Smatlak CR, Gossett JM, Zinder SH (1996) Comparative kinetics of hydrogen utilization for reductive dechlorination of tetrachloroethene and methanogenesis in an anaerobic enrichment culture. Environ Sci Technol 30(9):2850–2858CrossRefGoogle Scholar
  40. Strycharz SM, Woodard TL, Johnson JP, Nevin KP, Sanford RA, Loffler FE, Lovley DR (2008) Graphite electrode as a sole electron donor for reductive dechlorination of tetrachlorethene by Geobacter lovleyi. Appl Environ Microbiol 74(19):5943–5947CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 Rep 2(2):289–294CrossRefPubMedGoogle Scholar
  42. 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(6009):1413–1415CrossRefPubMedGoogle Scholar
  43. Sun M, Yan F, Zhang RL, Reible DD, Lowry GV, Gregory KB (2010) Redox control and hydrogen production in sediment caps using carbon cloth electrodes. Environ Sci Technol 44(21):8209–8215CrossRefPubMedPubMedCentralGoogle Scholar
  44. Sun JZ, Kingori GP, Si RW, Zhai DD, Liao ZH, Sun DZ, Zheng T, Yong YC (2015) Microbial fuel cell-based biosensors for environmental monitoring: a review. Water Sci Technol 71(6):801–809CrossRefPubMedGoogle Scholar
  45. Trombly J (1994) Electrochemical remediation takes to the field. Environ Sci Technol 28(6):A289–A291CrossRefGoogle Scholar
  46. Villano M, De Bonis L, Rossetti S, Aulenta F, Majone M (2011) Bioelectrochemical hydrogen production with hydrogenophilic dechlorinating bacteria as electrocatalytic agents. Bioresour Technol 102(3):3193–3199CrossRefPubMedGoogle Scholar
  47. Zhang RL, Lu XX, Reible DD, Jiao GZ, Qin SY (2013) Cathodic hydrogen as electron donor in enhanced reductive dechlorination. Chin J Chem Eng 21(12):1386–1390CrossRefGoogle Scholar
  48. Zhang DD, Zhang CF, Li ZL, Suzuki D, Komatsu DD, Tsunogai U, Katayama A (2014) Electrochemical stimulation of microbial reductive dechlorination of pentachlorophenol using solid-state redox mediator (humin) immobilization. Bioresour Technol 164:232–240CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Federico Aulenta
    • 1
    Email author
  • Simona Rossetti
    • 1
  • Bruna Matturro
    • 1
  • Valter Tandoi
    • 1
  • Roberta Verdini
    • 2
  • Mauro Majone
    • 2
  1. 1.Water Research Institute (IRSA), National Research Council (CNR)RomeItaly
  2. 2.Department of ChemistrySapienza University of RomeRomeItaly

Personalised recommendations