Advertisement

Current Microbiology

, Volume 75, Issue 1, pp 99–106 | Cite as

The Functional Mechanisms and Application of Electron Shuttles in Extracellular Electron Transfer

  • Bin Huang
  • Shumei Gao
  • Zhixiang Xu
  • Huan He
  • Xuejun Pan
Review Article

Abstract

Electron shuttles extensively exist in various environments. Some kinds of organic substances can be applied by microorganisms to produce electrons, and then the electrons can be transferred to other substances or microorganisms through electron shuttles, resulting in coexistence and interaction of diverse species of microbes. In this review, the functional mechanisms of extracellular electron transfer mediated by different electron shuttles are described. And different subtypes as well as the application of electron shuttles in microbial degradation of pollutants, microbial electricity, and the promotion of energy generation are also discussed. Summary results show that extracellular electron transfer is based on the electrogenesis microorganism with the structure of cytochromes or pili. Materials were usually used in long-distance electron transfer because of their widespread presence and abundance. Therefore, the review is beneficial to perceive the pathways of extracellular electron transfer mediated by electron shuttles and explore the contribution of different electron shuttles in extracellular electron transfer.

Keywords

Microorganisms Extracellular electron transfer Electron shuttles Application 

Notes

Acknowledgements

Funding was provided by the National Natural Science Foundation of China (Grant No. 41401558).

References

  1. 1.
    Aeschbacher M, Sander M, Schwarzenbach RP (2009) Novel electrochemical approach to assess the redox properties of humic substances. Environ Sci Technol 44:87–93CrossRefGoogle Scholar
  2. 2.
    Aeschbacher M, Vergari D, Schwarzenbach RP, Sander M (2011) Electrochemical analysis of proton and electron transfer equilibria of the reducible moieties in humic acids. Environ Sci Technol 45:8385–8394CrossRefPubMedGoogle Scholar
  3. 3.
    Blodau C, Bauer M, Regenspurg S, Macalady D (2009) Electron accepting capacity of dissolved organic matter as determined by reaction with metallic zinc. Chem Geol 260:186–195CrossRefGoogle Scholar
  4. 4.
    Blyth AW (1879) LVI.—The composition of cows’ milk in health and disease. J Chem Soc Trans 35:530–539CrossRefGoogle Scholar
  5. 5.
    Bond DR, Strycharz-Glaven SM, Tender LM, Torres CI (2012) On electron transport through Geobacter biofilms. ChemSusChem 5:1099–1105CrossRefPubMedGoogle Scholar
  6. 6.
    Boone DR, Johnson RL, Liu Y (1989) Diffusion of the interspecies electron carriers H2 and formate in methanogenic ecosystems and its implications in the measurement of Km for H2 or formate uptake. Appl Environ Microb 55:1735–1741Google Scholar
  7. 7.
    Breuer M, Rosso KM, Blumberger J, Butt JN (2015) Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities. J R Soc Interface 12:20141117CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 93:41–48CrossRefPubMedGoogle Scholar
  9. 9.
    Bryant M, Wolin E, Wolin M, Wolfe R (1967) Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch Microbiol 59:20–31Google Scholar
  10. 10.
    Chen J-J, Chen W, He H, Li D-B, Li W-W, Xiong L, Yu H-Q (2012) Manipulation of microbial extracellular electron transfer by changing molecular structure of phenazine-type redox mediators. Environ Sci Technol 47:1033–1039CrossRefPubMedGoogle Scholar
  11. 11.
    Chen S, Rotaru A-E, Shrestha PM, Malvankar NS, Liu F, Fan W, Nevin KP, Lovley DR (2014). Promoting interspecies electron transfer with biochar. Sci Rep 4:5019CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Coates JD, Cole KA, Chakraborty R, O’Connor SM, Achenbach LA (2002) Diversity and ubiquity of bacteria capable of utilizing humic substances as electron donors for anaerobic respiration. Appl Environ Microbiol 68:2445–2452CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    da Silva SM, Pacheco I, Pereira IAC (2012) Electron transfer between periplasmic formate dehydrogenase and cytochromes c in Desulfovibrio desulfuricans ATCC 27774. J Biol Inorg Chem 17:831–838CrossRefPubMedGoogle Scholar
  14. 14.
    Das S, Mishra J, Das SK, Pandey S, Rao DS, Chakraborty A, Sudarshan M, Das N, Thatoi H (2014) Investigation on mechanism of Cr (VI) reduction and removal by Bacillus amyloliquefaciens, a novel chromate tolerant bacterium isolated from chromite mine soil. Chemosphere 96:112–121CrossRefPubMedGoogle Scholar
  15. 15.
    Dong G, Zhang L (2013) Synthesis and enhanced Cr (VI) photoreduction property of formate anion containing graphitic carbon nitride. J Phys Chem C 117:4062–4068CrossRefGoogle Scholar
  16. 16.
    Edwards MJ, White GF, Norman M, Tome-Fernandez A, Ainsworth E, Shi L, Fredrickson JK, Zachara JM, Butt JN, Richardson DJ (2015) Redox linked flavin sites in extracellular decaheme proteins involved in microbe-mineral electron transfer. Sci Rep 5:11677CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    El Fantroussi S, Naveau H, Agathos SN (1998) Anaerobic dechlorinating bacteria. Biotechnol Prog 14:167–188CrossRefPubMedGoogle Scholar
  18. 18.
    Hashsham SA, Freedman DL (1999) Enhanced biotransformation of carbon tetrachloride by Acetobacterium woodii upon addition of hydroxocobalamin and fructose. Appl Environ Microbiol 65:4537–4542PubMedPubMedCentralGoogle Scholar
  19. 19.
    Hassan HM, Fridovich I (1980) Mechanism of the antibiotic action pyocyanine. J Bacteriol 141:156–163PubMedPubMedCentralGoogle Scholar
  20. 20.
    Hassett D, Charniga L, Bean K, Ohman D, Cohen M (1992) Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect Immun 60:328–336PubMedPubMedCentralGoogle Scholar
  21. 21.
    Hattori S, Luo H, Shoun H, Kamagata Y (2001) Involvement of formate as an interspecies electron carrier in a syntrophic acetate-oxidizing anaerobic microorganism in coculture with methanogens. J Biosci Bioeng 91:294–298CrossRefPubMedGoogle Scholar
  22. 22.
    Holliger C, Wohlfarth G, Diekert G (1998) Reductive dechlorination in the energy metabolism of anaerobic bacteria. FEMS Microbiol Rev 22:383–398CrossRefGoogle Scholar
  23. 23.
    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 8:1805–1815CrossRefPubMedGoogle Scholar
  24. 24.
    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 76:3999–4007CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Jayapriya J, Ramamurthy V (2012) Use of non-native phenazines to improve the performance of Pseudomonas aeruginosa MTCC 2474 catalysed fuel cells. Bioresource Technol 124:23–28CrossRefGoogle Scholar
  26. 26.
    Kato S, Hashimoto K, Watanabe K (2012) Microbial interspecies electron transfer via electric currents through conductive minerals. Proc Natl Acad Sci India B 109:10042–10046Google Scholar
  27. 27.
    Keller L, Surette MG (2006) Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4:249CrossRefPubMedGoogle Scholar
  28. 28.
    Klüpfel L, Piepenbrock A, Kappler A, Sander M (2014) Humic substances as fully regenerable electron acceptors in recurrently anoxic environments. Nat Geosci 7:195CrossRefGoogle Scholar
  29. 29.
    Kokhan O, Ponomarenko NS, Pokkuluri PR, Schiffer M, Mulfort KL, Tiede DM (2015) Bidirectional photoinduced electron transfer in ruthenium (II)-tris-bipyridyl-modified PpcA, a multi-heme c-type cytochrome from Geobacter sulfurreducens. J Phys Chem B 119:7612–7624CrossRefPubMedGoogle Scholar
  30. 30.
    Kotloski NJ, Gralnick JA (2013) Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. MBio 4:e00553-00512CrossRefGoogle Scholar
  31. 31.
    Larsen Ø, Karlsen OA (2016) Transcriptomic profiling of Methylococcus capsulatus (Bath) during growth with two different methane monooxygenases. Microbiologyopen 5:254–267CrossRefPubMedGoogle Scholar
  32. 32.
    Lau GW, Hassett DJ, Ran H, Kong F (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10:599–606CrossRefPubMedGoogle Scholar
  33. 33.
    Lau GW, Ran H, Kong F, Hassett DJ, Mavrodi D (2004) Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect Immun 72:4275–4278CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Leang C, Qian X, Mester T, Lovley DR (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl Environ Microbiol 76:4080–4084CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Lee Y, Bae S, Moon C, Lee W (2015) Flavin mononucleotide mediated microbial fuel cell in the presence of Shewanella putrefaciens CN32 and iron-bearing mineral. Biotechnol Bioprocess Eng 20:894–900CrossRefGoogle Scholar
  36. 36.
    Li M, Su Y, Chen Y, Wan R, Zheng X, Liu K (2016) The effects of fulvic acid on microbial denitrification: promotion of NADH generation, electron transfer, and consumption. Appl Microbiol Biotechnol 100:5607–5618CrossRefPubMedGoogle Scholar
  37. 37.
    Li W-W, Yu H-Q, He Z (2014) Towards sustainable wastewater treatment by using microbial fuel cells-centered technologies. Energy Environ Sci 7:911–924CrossRefGoogle Scholar
  38. 38.
    Li X, Liu L, Liu T, Yuan T, Zhang W, Li F, Zhou S, Li Y (2013) Electron transfer capacity dependence of quinone-mediated Fe (III) reduction and current generation by Klebsiella pneumoniae L17. Chemosphere 92:218–224CrossRefPubMedGoogle Scholar
  39. 39.
    Liu G, Qiu S, Liu B, Pu Y, Gao Z, Wang J, Jin R, Zhou J (2017). Microbial reduction of Fe (III)-bearing clay minerals in the presence of humic acids. Sci Rep 7:45354CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Liu T, Li X, Li F, Han R, Wu Y, Yuan X, Wang Y (2016). In situ spectral kinetics of Cr (VI) reduction by c-type cytochromes in a suspension of living Shewanella putrefaciens 200. Sci Rep 6:29592CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Lovley DR (2012) Long-range electron transport to Fe (III) oxide via pili with metallic-like conductivity. Biochem Soc Trans 40:1186–1190 (Portland Press Limited)CrossRefGoogle Scholar
  42. 42.
    Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJ, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445CrossRefGoogle Scholar
  43. 43.
    Lu Q, Yuan Y, Tao Y, Tang J (2015) Environmental pH and ionic strength influence the electron-transfer capacity of dissolved organic matter. J Soil Sediment 15:2257–2264CrossRefGoogle Scholar
  44. 44.
    Malvankar NS, Lovley DR (2014) Microbial nanowires for bioenergy applications. Curr Opin Biotechnol 27:88–95CrossRefPubMedGoogle Scholar
  45. 45.
    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 78:173–175CrossRefPubMedGoogle Scholar
  46. 46.
    McKenzie AM (2016) Ultrafast limits of photo-induced electron transfer rates in PPCA, a multi-heme C-type cytochrome. Biophys J 110:18aCrossRefGoogle Scholar
  47. 47.
    Mehta T, Coppi MV, Childers SE, Lovley DR (2005) Outer membrane c-type cytochromes required for Fe (III) and Mn (IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol 71:8634–8641CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Moran JJ, Beal EJ, Vrentas JM, Orphan VJ, Freeman KH, House CH (2008) Methyl sulfides as intermediates in the anaerobic oxidation of methane. Environ Microbiol 10:162–173PubMedGoogle Scholar
  49. 49.
    Mountfort D, Brulla W, Krumholz LR, Bryant M (1984) Syntrophus buswellii gen. nov., sp. nov.: a benzoate catabolizer from methanogenic ecosystems. Int J Syst Evol Microbiol 34:216–217Google Scholar
  50. 50.
    Nevin KP, Kim B-C, Glaven RH, Johnson JP, Woodard TL, Methé BA, DiDonato RJ Jr, Covalla SF, Franks AE, Liu A (2009) Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PloS ONE 4:e5628CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Orsetti S, Laskov C, Haderlein SB (2013) Electron transfer between iron minerals and quinones: estimating the reduction potential of the Fe (II)-goethite surface from AQDS speciation. Environ Sci Technol 47:14161–14168CrossRefPubMedGoogle Scholar
  52. 52.
    Paquete CM, Fonseca BM, Cruz DR, Pereira TM, Pacheco I, Soares CM, Louro RO (2014). Exploring the molecular mechanisms of electron shuttling across the microbe/metal space. Front Microbiol 5:318CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Pokkuluri P, Londer Y, Yang X, Duke N, Erickson J, Orshonsky V, Johnson G, Schiffer M (2010) Structural characterization of a family of cytochromes c 7 involved in Fe (III) respiration by Geobacter sulfurreducens. BBA-Bioenergetics 1797:222–232CrossRefPubMedGoogle Scholar
  54. 54.
    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 1807:404–412CrossRefPubMedGoogle Scholar
  55. 55.
    Qian X, Reguera G, Mester T, Lovley DR (2007) Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins. FEMS Microbiol Lett 277:21–27CrossRefPubMedGoogle Scholar
  56. 56.
    Rabaey K, Boon N, Höfte M, Verstraete W (2005) Microbial phenazine production enhances electron transfer in biofuel cells. Environ Sci Technol 39:3401–3408CrossRefPubMedGoogle Scholar
  57. 57.
    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 70:5373–5382CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Reguera G (2015) Microbes, cables, and an electrical touch. Int Microbiol 18:151–157PubMedGoogle Scholar
  59. 59.
    Reguera G, McCarthy KD, Mehta T, Nicoll JS (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098CrossRefPubMedGoogle Scholar
  60. 60.
    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 72:7345–7348CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Richter LV, Franks AE, Weis RM, Sandler SJ (2017) Significance of a posttranslational modification of the PilA protein of Geobacter sulfurreducens for surface attachment, biofilm formation, and growth on insoluble extracellular electron acceptors. J Bacteriol 199:e00716–e00716CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Roden EE, Kappler A, Bauer I, Jiang J, Paul A, Stoesser R, Konishi H, Xu H (2010) Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat Geosci 3:417–421CrossRefGoogle Scholar
  63. 63.
    Rotaru A-E, Shrestha PM, Liu F, Ueki T, Nevin K, Summers ZM, Lovley DR (2012) Interspecies electron transfer via hydrogen and formate rather than direct electrical connections in cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens. Appl Environ Microbiol 78:7645–7651CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Santos TC, Silva MA, Morgado L, Dantas JM, Salgueiro CA (2015) Diving into the redox properties of Geobacter sulfurreducens cytochromes: a model for extracellular electron transfer. Dalton Trans 44:9335–9344CrossRefPubMedGoogle Scholar
  65. 65.
    Saratale RG, Saratale GD, Chang J-S, Govindwar S (2011) Bacterial decolorization and degradation of azo dyes: a review. J Taiwan Inst Chem E 42:138–157CrossRefGoogle Scholar
  66. 66.
    Schmidt JE, Ahring BK (1995) Interspecies electron transfer during propionate and butyrate degradation in mesophilic, granular sludge. Appl Environ Microbiol 61:2765–2767PubMedPubMedCentralGoogle Scholar
  67. 67.
    Schmitz S, Nies S, Wierckx N, Blank LM, Rosenbaum MA (2015). Engineering mediator-based electroactivity in the obligate aerobic bacterium Pseudomonas putida KT2440. Front Microbiol 6:284CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Scott DT, McKnight DM, Blunt-Harris EL, Kolesar SE, Lovley DR (1998) Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ Sci Technol 32:2984–2989CrossRefGoogle Scholar
  69. 69.
    Shelobolina ES, Coppi MV, Korenevsky AA, DiDonato LN, Sullivan SA, Konishi H, Xu H, Leang C, Butler JE, Kim B-C (2007) Importance of c-type cytochromes for U (VI) reduction by Geobacter sulfurreducens. BMC Microbiol 7:16CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Shrestha PM, Rotaru A-E, Summers ZM, Shrestha M, Liu F, Lovley DR (2013) Transcriptomic and genetic analysis of direct interspecies electron transfer. Appl Environ Microbiol 79:2397–2404CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Sieber JR, Sims DR, Han C, Kim E, Lykidis A, Lapidus AL, McDonnald E, Rohlin L, Culley DE, Gunsalus R (2010) The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production. Environ Microbiol 12:2289–2301PubMedGoogle Scholar
  72. 72.
    Stams AJ, De Bok FA, Plugge CM, Eekert V, Miriam H, Dolfing J, Schraa G (2006) Exocellular electron transfer in anaerobic microbial communities. Environ Microbiol 8:371–382CrossRefPubMedGoogle Scholar
  73. 73.
    Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM (2011) On the electrical conductivity of microbial nanowires and biofilms. Energy Environ Sci 4:4366–4379CrossRefGoogle Scholar
  74. 74.
    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 80:142–150CrossRefPubMedGoogle Scholar
  75. 75.
    Tang J, Liu Y, Yuan Y, Zhou S (2014) Humic acid-enhanced electron transfer of in vivo cytochrome c as revealed by electrochemical and spectroscopic approaches. J Environ Sci 26:1118–1124CrossRefGoogle Scholar
  76. 76.
    Thiele JH, Zeikus JG (1988) Control of interspecies electron flow during anaerobic digestion: significance of formate transfer versus hydrogen transfer during syntrophic methanogenesis in flocs. Appl Environ Microbiol 54:20–29PubMedPubMedCentralGoogle Scholar
  77. 77.
    Van der Zee FP, Villaverde S (2005) Combined anaerobic–aerobic treatment of azo dyes—a short review of bioreactor studies. Water Res 39:1425–1440CrossRefPubMedGoogle Scholar
  78. 78.
    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
  79. 79.
    Wang L, Su L, Chen H, Yin T, Lin Z, Lin X, Fu D (2015) Carbon paper electrode modified by goethite nanowhiskers promotes bacterial extracellular electron transfer. Mater Lett 141:311–314CrossRefGoogle Scholar
  80. 80.
    Watanabe K, Manefield M, Lee M, Kouzuma A (2009) Electron shuttles in biotechnology. Curr Opin Biotechnol 20:633–641CrossRefPubMedGoogle Scholar
  81. 81.
    Xu S, Jangir Y, El-Naggar MY (2016) Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1. Electrochim Acta 198:49–55CrossRefGoogle Scholar
  82. 82.
    Xu Y-S, Zheng T, Yong X-Y, Zhai D-D, Si R-W, Li B, Yu Y-Y, Yong Y-C (2016) Trace heavy metal ions promoted extracellular electron transfer and power generation by Shewanella in microbial fuel cells. Bioresource Technol 211:542–547CrossRefGoogle Scholar
  83. 83.
    Yang Y, Ding Y, Hu Y, Cao B, Rice SA, Kjelleberg S, Song H (2015) Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway. ACS Synth Biol 4:815–823CrossRefPubMedGoogle Scholar
  84. 84.
    Yin Q, Hu Z, Sun Y, Li B, Wu G (2017). Effect of the dosage of ferroferric oxide on batch anaerobic treatment of high strengthen synthetic wastewater. In Proceedings of The 13th IWA Specialized Conference on Small Water and Wastewater Systems and the 5th IWA Specialized Conference on Resources-Oriented Sanitation. http://uest.ntua.gr/swws/proceedings/pdf/Qidong_Yin_et_al.pdf. Accessed, Volume 11
  85. 85.
    Yin Q, Miao J, Li B, Wu G (2017) Enhancing electron transfer by ferroferric oxide during the anaerobic treatment of synthetic wastewater with mixed organic carbon. Int Biodeter Biodegr 119:104–110CrossRefGoogle Scholar
  86. 86.
    You S, Ma M, Wang W, Qi D, Chen X, Qu J, Ren N (2017). 3D macroporous nitrogen-enriched graphitic carbon scaffold for efficient bioelectricity generation in microbial fuel cells. Adv Energy Mater.  https://doi.org/10.1002/aenm.201601364 Google Scholar
  87. 87.
    Yu Z-G, Orsetti S, Haderlein SB, Knorr K-H (2016) Electron transfer between sulfide and humic acid: electrochemical evaluation of the reactivity of Sigma-Aldrich humic acid toward sulfide. Aquat Geochem 22:117–130CrossRefGoogle Scholar
  88. 88.
    Yuan T, Yuan Y, Zhou S, Li F, Liu Z, Zhuang L (2011) A rapid and simple electrochemical method for evaluating the electron transfer capacities of dissolved organic matter. J Soil Sediment 11:467–473CrossRefGoogle Scholar
  89. 89.
    Zhang C, Katayama A (2012) Humin as an electron mediator for microbial reductive dehalogenation. Environ Sci Technol 46:6575–6583CrossRefPubMedGoogle Scholar
  90. 90.
    Zhao Z, Zhang Y, Li Y, Dang Y, Zhu T, Quan X (2017) Potentially shifting from interspecies hydrogen transfer to direct interspecies electron transfer for syntrophic metabolism to resist acidic impact with conductive carbon cloth. Chem Eng J 313:10–18CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Bin Huang
    • 1
  • Shumei Gao
    • 1
  • Zhixiang Xu
    • 1
  • Huan He
    • 1
  • Xuejun Pan
    • 1
  1. 1.Faculty of Environmental Science and EngineeringKunming University of Science and TechnologyKunmingPeople’s Republic of China

Personalised recommendations