Advertisement

Electron Transfer Between Enzymes and Electrodes

  • Tanja Vidakovic-KochEmail author
Chapter
Part of the Advances in Biochemical Engineering/Biotechnology book series (ABE, volume 167)

Abstract

Efficient electron transfer between redox enzymes and electrocatalytic surfaces plays a significant role in development of novel energy conversion devices as well as novel reactors for production of commodities and fine chemicals. Major application examples are related to enzymatic fuel cells and electroenzymatic reactors, as well as enzymatic biosensors. The two former applications are still at the level of proof-of-concept, partly due to the low efficiency and obstacles to electron transfer between enzymes and electrodes. This chapter discusses the theoretical backgrounds of enzyme/electrode interactions, including the main mechanisms of electron transfer, as well as thermodynamic and kinetic aspects. Additionally, the main electrochemical methods of study are described for selected examples. Finally, some recent advancements in the preparation of enzyme-modified electrodes as well as electrodes for soluble co-factor regeneration are reviewed.

Graphical Abstract

Keywords

Direct electron transfer Electrochemical co-factor regeneration Electrochemical methods Kinetics Mediated electron transfer Porous electrodes Redox enzymes 

References

  1. 1.
    Copeland RA (2000) Enzyme reactions with multiple substrates. In: Enzymes: a practical introduction to structure, mechanism, and data analysis, 2nd edn. Wiley, New York, pp 350–366Google Scholar
  2. 2.
    Vidakovic-Koch T, Sundmacher K (2017) Porous electrodes in bioelectrochemistry. In: V P (ed) Encyclopedia of interfacial chemistry: surface science and electrochemistry, Elsevier, AmsterdamGoogle Scholar
  3. 3.
    Belsare KD et al (2017) Directed evolution of P450cin for mediated electron transfer. Protein Eng Des Sel 30(2):119–127PubMedGoogle Scholar
  4. 4.
    Habermüller K, Mosbach M, Schuhmann W (2000) Electron-transfer mechanisms in amperometric biosensors. Fresenius J Anal Chem 366(6):560–568PubMedGoogle Scholar
  5. 5.
    Do TQN et al (2014) Mathematical modeling of a porous enzymatic electrode with direct electron transfer mechanism. Electrochim Acta 137:616–626Google Scholar
  6. 6.
    Andreu R et al (2007) Direct electron transfer kinetics in horseradish peroxidase electrocatalysis. J Phys Chem B 111(2):469–477PubMedGoogle Scholar
  7. 7.
    Gupta G et al (2011) Direct electron transfer catalyzed by bilirubin oxidase for air breathing gas-diffusion electrodes. Electrochem Commun 13(3):247–249Google Scholar
  8. 8.
    Léger C et al (2002) Effect of a dispersion of interfacial electron transfer rates on steady state catalytic electron transport in [NiFe]-hydrogenase and other enzymes. J Phys Chem B 106(50):13058–13063Google Scholar
  9. 9.
    Tasca F et al (2008) Direct electron transfer at cellobiose dehydrogenase modified anodes for biofuel cells. J Phys Chem C 112(26):9956–9961Google Scholar
  10. 10.
    Zimmermann H et al (2000) Anisotropic orientation of horseradish peroxidase by reconstitution on a Thiol-modified gold electrode. Chem Eur J 6(4):592–599PubMedGoogle Scholar
  11. 11.
    Vidaković-Koch T et al (2011) Impact of the gold support on the electrocatalytic oxidation of sugars at enzyme-modified electrodes. Electroanalysis 23(4):927–930Google Scholar
  12. 12.
    Courjean O, Gao F, Mano N (2009) Deglycosylation of glucose oxidase for direct and efficient glucose electrooxidation on a glassy carbon electrode. Angew Chem 121(32):6011–6013Google Scholar
  13. 13.
    Bartlett PN, Al-Lolage FA (2017) There is no evidence to support literature claims of direct electron transfer (DET) for native glucose oxidase (GOx) at carbon nanotubes or graphene. J Electroanal ChemGoogle Scholar
  14. 14.
    Alberty RA (1993) Thermodynamics of reactions of Nicotinamide adenine dinucleotide and Nicotinamide adenine dinucleotide phosphate. Arch Biochem Biophys 307(1):8–14PubMedGoogle Scholar
  15. 15.
    Krebs HA, Kornberg HL (1957) Energy transformations in living matter. Springer-Verlag Berlin Heidelberg, BerlinGoogle Scholar
  16. 16.
    Reiger PH (1994) Electrochemistry.2nd edn. Springer Science+Business Media, DordrechtGoogle Scholar
  17. 17.
    Armstrong FA, Hirst J (2011) Reversibility and efficiency in electrocatalytic energy conversion and lessons from enzymes. Proc Natl Acad Sci 108(34):14049–14054PubMedGoogle Scholar
  18. 18.
    Togo M et al (2007) An enzyme-based microfluidic biofuel cell using vitamin K3-mediated glucose oxidation. Electrochim Acta 52(14):4669–4674Google Scholar
  19. 19.
    Mano N, Mao F, Heller A (2002) A miniature biofuel cell operating in a physiological buffer. J Am Chem Soc 124(44):12962–12963PubMedGoogle Scholar
  20. 20.
    Chen T et al (2001) A miniature biofuel cell. J Am Chem Soc 123(35):8630–8631PubMedGoogle Scholar
  21. 21.
    Kim H-H et al (2003) A miniature membrane-less biofuel cell operating under physiological conditions at 0.5 V. J Electrochem Soc 150(2):A209–A213Google Scholar
  22. 22.
    Willner I et al (1998) Biofuel cell based on glucose oxidase and microperoxidase-11 monolayer-functionalized electrodes. J Chem Soc Perkin Trans 2(8):1817–1822Google Scholar
  23. 23.
    Kuwahara T et al (2007) Properties of the enzyme electrode fabricated with a film of polythiophene derivative and its application to a glucose fuel cell. J Appl Polym Sci 104(5):2947–2953Google Scholar
  24. 24.
    Brunel L et al (2007) Oxygen transport through laccase biocathodes for a membrane-less glucose/O2 biofuel cell. Electrochem Commun 9(2):331–336Google Scholar
  25. 25.
    Bedekar AS et al (2007) Oxygen limitation in microfluidic biofuel cells. Chem Eng Commun 195(3):256–266Google Scholar
  26. 26.
    Nazaruk E et al (2008) Enzymatic biofuel cell based on electrodes modified with lipid liquid-crystalline cubic phases. J Power Sources 183(2):533–538Google Scholar
  27. 27.
    Tamaki T, Yamaguchi T (2006) High-surface-area three-dimensional biofuel cell electrode using redox-polymer-grafted carbon. Ind Eng Chem Res 45(9):3050–3058Google Scholar
  28. 28.
    Matsue T et al (1985) Electron-transfer reactions associated with host-guest complexation. Oxidation of ferrocenecarboxylic acid in the presence of .beta.-cyclodextrin. J Am Chem Soc 107(12):3411–3417Google Scholar
  29. 29.
    Yan Y-M, Yehezkeli O, Willner I (2007) Integrated, electrically contacted NAD(P)+−dependent enzyme–carbon nanotube electrodes for biosensors and biofuel cell applications. Chem Eur J 13(36):10168–10175PubMedGoogle Scholar
  30. 30.
    Li X et al (2008) A miniature glucose/O2 biofuel cell with single-walled carbon nanotubes-modified carbon fiber microelectrodes as the substrate. Electrochem Commun 10(6):851–854Google Scholar
  31. 31.
    Gao F et al (2007) An enzymatic glucose/O2 biofuel cell: preparation, characterization and performance in serum. Electrochem Commun 9(5):989–996Google Scholar
  32. 32.
    Yan Y et al (2006) Carbon-nanotube-based glucose/O2 biofuel cells. Adv Mater 18(19):2639–2643Google Scholar
  33. 33.
    Vidaković-Koch T et al (2013) Application of electrochemical impedance spectroscopy for studying of enzyme kinetics. Electrochim Acta 110:94–104Google Scholar
  34. 34.
    Vidaković-Koch TR et al (2011) Nonlinear frequency response analysis of the Ferrocyanide oxidation kinetics. Part I. A theoretical analysis. J Phys Chem C 115(35):17341–17351Google Scholar
  35. 35.
    Do TQN et al (2015) Dynamic and steady state 1-D model of mediated electron transfer in a porous enzymatic electrode. Bioelectrochemistry 106(Part A):3–13PubMedGoogle Scholar
  36. 36.
    Vidaković-Koch T et al (2017) Catalyst layer modeling. In: Breitkopf C, Swider-Lyons K (eds) Springer handbook of electrochemical energy. Springer Berlin Heidelberg, Berlin, pp 259–285Google Scholar
  37. 37.
    Bard A, Faulkner L (2001) Electrochemical methods, fundamentals and applications. Wiley, New YorkGoogle Scholar
  38. 38.
    Bartlett PN (2008) In: Bartlett PN (ed) Bioelectrochemistry: fundamentals, experimental techniques and applications. Wiley, New YorkGoogle Scholar
  39. 39.
    Varnicic M et al (2014) Combined electrochemical and microscopic study of porous enzymatic electrodes with direct electron transfer mechanism. RSC Adv 4(69):36471–36479Google Scholar
  40. 40.
    Varničić M, Vidaković-Koch T, Sundmacher K (2015) Gluconic acid synthesis in an electroenzymatic reactor. Electrochim Acta 174:480–487Google Scholar
  41. 41.
    Varničić M, Vidaković-Koch T, Sundmacher K (2015) Corrigendum to “Gluconic acid synthesis in an Electroenzymatic reactor” [Electrochimica Acta 174 (2015) 480–487]. Electrochim Acta 176:1523Google Scholar
  42. 42.
    Ivanov I (2012) Development of a glucose-oxygen enzymatic fuel cell. Otto von Guericke University, Magdeburg, p 118Google Scholar
  43. 43.
    Ivanov I, Vidaković-Koch T, Sundmacher K (2013) Alternating electron transfer mechanism in the case of high-performance tetrathiafulvalene–tetracyanoquinodimethane enzymatic electrodes. J Electroanal Chem 690:68–73Google Scholar
  44. 44.
    Vidakovic-Koch T (2017) Energy conversion based on bio(electro)catalysts. In: Cornelia Breitkopf KS-L (ed) Springer handbook of electrochemical energy. Springer-Verlag Berlin Heidelberg, Berlin, pp 757–777Google Scholar
  45. 45.
    Mondal MS, Fuller HA, Armstrong FA (1996) Direct measurement of the reduction potential of catalytically active cytochrome c peroxidase compound I: voltammetric detection of a reversible, cooperative two-electron transfer reaction. J Am Chem Soc 118(1):263–264Google Scholar
  46. 46.
    Mondal MS, Goodin DB, Armstrong FA (1998) Simultaneous voltammetric comparisons of reduction potentials, reactivities, and stabilities of the high-potential catalytic states of wild-type and distal-pocket mutant (W51F) yeast cytochrome c peroxidase. J Am Chem Soc 120(25):6270–6276Google Scholar
  47. 47.
    Ruzgas T et al (1995) Kinetic models of horseradish peroxidase action on a graphite electrode. J Electroanal Chem 391(1):41–49Google Scholar
  48. 48.
    Ferapontova EE, Gorton L (2001) Effect of proton donors on direct electron transfer in the system gold electrode–horseradish peroxidase. Electrochem Commun 3(12):767–774Google Scholar
  49. 49.
    Yu H et al (2015) Influence of the ionomer/carbon ratio for low-Pt loading catalyst layer prepared by reactive spray deposition technology. J Power Sources 283:84–94Google Scholar
  50. 50.
    Lojou É, Bianco P (2004) Membrane electrodes for protein and enzyme electrochemistry. Electroanalysis 16(13–14):1113–1121Google Scholar
  51. 51.
    De Poulpiquet A et al (2013) Exploring properties of a hyperthermophilic membrane-bound hydrogenase at carbon nanotube modified electrodes for a powerful H2/O2 biofuel cell. Electroanalysis 25(3):685–695Google Scholar
  52. 52.
    Lojou É et al (2008) Biocatalysts for fuel cells: efficient hydrogenase orientation for H2 oxidation at electrodes modified with carbon nanotubes. JBIC, J Biol Inorg Chem 13(7):1157–1167PubMedGoogle Scholar
  53. 53.
    Luo X et al (2009) Immobilization of the hyperthermophilic hydrogenase from Aquifex aeolicus bacterium onto gold and carbon nanotube electrodes for efficient H2 oxidation. JBIC, J Biol Inorg Chem 14(8):1275–1288PubMedGoogle Scholar
  54. 54.
    Lojou E (2011) Hydrogenases as catalysts for fuel cells: strategies for efficient immobilization at electrode interfaces. Electrochim Acta 56(28):10385–10397Google Scholar
  55. 55.
    Yan Y, Su L, Mao L (2007) Multi-walled carbon nanotube-based glucose/O2 biofuel cell with glucose oxidase and Laccase as biocatalysts. J Nanosci Nanotechnol 7(4–1):1625–1630PubMedGoogle Scholar
  56. 56.
    Khan GF (1997) TTF-TCNQ complex based printed biosensor for long-term operation. Electroanalysis 9(4):325–329Google Scholar
  57. 57.
    Khan GF (1996) Construction of SEC/CTC electrodes for direct electron transferring biosensors. Sens Actuators B Chem 36(1–3):484–490Google Scholar
  58. 58.
    Khan GF, Ohwa M, Wernet W (1996) Design of a stable charge transfer complex electrode for a third-generation amperometric glucose sensor. Anal Chem 68(17):2939–2945PubMedGoogle Scholar
  59. 59.
    Ivanov I, Vidaković-Koch T, Sundmacher K (2011) Direct hybrid glucose–oxygen enzymatic fuel cell based on tetrathiafulvalene–tetracyanoquinodimethane charge transfer complex as anodic mediator. J Power Sources 196(22):9260–9269Google Scholar
  60. 60.
    Do TQN (2017) Mathematical modelling of electro-enzymatic system. Otto von Guericke University, MagdeburgGoogle Scholar
  61. 61.
    Kochius S et al (2014) Electrochemical regeneration of oxidised nicotinamide cofactors in a scalable reactor. J Mol Catal B Enzym 103:94–99Google Scholar
  62. 62.
    Gorton L, Domínguez E (2007) Electrochemistry of NAD(P)+/NAD(P)H. Encyclopedia of electrochemistry. Wiley-VCH Verlag GmbH & Co. KGaA, WeinheimGoogle Scholar
  63. 63.
    Karyakin AA, Ivanova YN, Karyakina EE (2003) Equilibrium (NAD+/NADH) potential on poly(neutral red) modified electrode. Electrochem Commun 5(8):677–680Google Scholar
  64. 64.
    Arechederra MN, Addo PK, Minteer SD (2011) Poly(neutral red) as a NAD+ reduction catalyst and a NADH oxidation catalyst: towards the development of a rechargeable biobattery. Electrochim Acta 56(3):1585–1590Google Scholar
  65. 65.
    Karyakin AA et al (1999) Electropolymerized azines: part II. In a search of the best electrocatalyst of NADH oxidation. Electroanalysis 11(8):553–557Google Scholar
  66. 66.
    Li H, Wen H, Calabrese Barton S (2012) NADH oxidation catalyzed by electropolymerized azines on carbon nanotube modified electrodes. Electroanalysis 24(2):398–406Google Scholar
  67. 67.
    Rincón RA et al (2011) Flow-through 3D biofuel cell anode for NAD+−dependent enzymes. Electrochim Acta 56(5):2503–2509Google Scholar
  68. 68.
    Vuorilehto K, Lütz S, Wandrey C (2004) Indirect electrochemical reduction of nicotinamide coenzymes. Bioelectrochemistry 65(1):1–7PubMedGoogle Scholar
  69. 69.
    Salimi A et al (2009) Electrocatalytic reduction of NAD+ at glassy carbon electrode modified with single-walled carbon nanotubes and Ru(III) complexes. J Solid State Electrochem 13(3):485–496Google Scholar
  70. 70.
    Ali I, Soomro B, Omanovic S (2011) Electrochemical regeneration of NADH on a glassy carbon electrode surface: the influence of electrolysis potential. Electrochem Commun 13(6):562–565Google Scholar
  71. 71.
    Tosstorff A et al (2014) Mediated electron transfer with monooxygenases—insight in interactions between reduced mediators and the co-substrate oxygen. J Mol Catal B Enzym 108:51–58Google Scholar
  72. 72.
    Tosstorff A et al (2017) Towards electroenzymatic processes involving old yellow enzymes and mediated cofactor regeneration. Eng Life Sci 17(1):71–76Google Scholar
  73. 73.
    Çekiç SZ et al (2010) Mediated electron transfer with P450cin. Electrochem Commun 12(11):1547–1550Google Scholar
  74. 74.
    Ströhle FW et al (2013) A computational protocol to predict suitable redox mediators for substitution of NAD(P)H in P450 monooxygenases. J Mol Catal B Enzym 88:47–51Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Max Planck Institute for Dynamics of Complex Technical SystemsMagdeburgGermany

Personalised recommendations