Kinetics of Mediated Bioelectrocatalytic Oxidation of Glucose by Protein Extracts of Escherichia coli

M. V. DmitrievaM. V. Dmitrieva, I. N. ShishovI. N. Shishov, S. V. ShmaliiS. V. Shmalii, V. D. MyazinV. D. Myazin, A. Yu. BazhenovA. Yu. Bazhenov, E. V. GerasimovaE. V. Gerasimova, E. V. ZolotukhinaE. V. Zolotukhina
Российский электрохимический журнал
Abstract / Full Text

The kinetics of bioelectrocatalytic oxidation of glucose by protein extracts—supersonic-destruction products of Escherichia coli BB cells—is studied in the presence of [Fe(CN)6]3– as the mediator system. The effect of the concentration of mediator, glucose, and protein extract is studied by electrochemical methods. The results are used in determination of effective parameters: the rate constant of glucose biooxidation, the constant of substrate-induced inhibition, and the activation energy. It is shown that the activation energy of this reaction falls into the interval of activation energies of dehydrogenase reactions. The voltammetric characteristics of a model asymmetrical biofuel cell which employs the protein extract as the anodic catalyst are determined. The maximum specific power of such model biofuel cell is found to be 400 µW/cm2 (4 W/m2).

Author information
  • Institute of Problems of Chemical Physics, Russian Academy of Sciences, 142432, Chernogolovka, Moscow oblast, RussiaM. V. Dmitrieva, E. V. Gerasimova & E. V. Zolotukhina
  • Moscow State University, Leninskie Gory, 119992, Moscow, RussiaI. N. Shishov, S. V. Shmalii, V. D. Myazin & A. Yu. Bazhenov
  • Moscow Institute of Physics and Technology, 141701, Dolgoprudnyi, Moscow oblast, RussiaE. V. Zolotukhina
  1. Cosnier, S., Gross, A.J., A. Le Goff, and Holzinger, M., Recent advances on enzymatic glucose/oxygen and hydrogen/oxygen biofuel cells: Achievements and limitations, J. Power Sources, 2016, vol. 325, p. 252.
  2. Rabaey, K., Boon, N., Höfte, M., and Verstraete, W., Microbial phenazine production enhances electron transfer in biofuel cells, Environ. Sci. Technol., 2005, vol. 39, p. 3401.
  3. Stoica, L., Ruzgas, T., Ludwig, R., Haltrich, D., and Gorton, L., Direct electron transfers a favorite electron route for cellobiose dehydrogenase (CDH) from Trametes v illosa. Comparison with CDH from Phanerochaete chrysosporium, Langmuir, 2006, vol. 22, p. 10801.
  4. Hickey, D.P., Milton, R.D., Rasmussen, M., Abdellaoui, S., Nguyen, K., and Minteer, S.D, Fundamentals and applications of bioelectrocatalysis, Electrochemistry, 2015, vol. 13, p. 97.
  5. Cooper, J. and Cass, A., Biosensors, New York: OUP Oxford, 2004, p. 59.
  6. Bartlett, P.N., Bioelectrochemistry: Fundamentals, Experimental Techniques and Applications, New York: Wiley, 2008.
  7. Bartlett, P.N. and Pratt, K.F.E., A study of the kinetics of the reaction between ferrocene monocarboxylic acid and glucose oxidase using the rotating-disc electrode, J. Electroanal. Chem., 1995, vol. 397, no. 1–2, p. 53.
  8. Alegret S., Integrated Analytical Systems, Amsterdam: Gulf Professional, 2003.
  9. Flexer, V., Ielmini, M.V., Calvo, E.J., and Bartlett, P.N., Extracting kinetic parameters for homogeneous [Os (bpy) 2ClPyCOOH]+ mediated enzyme reactions from cyclic voltammetry and simulations, Bioelectrochem., 2008, vol. 74, no. 1, p. 201.
  10. Hui, T.W., Wong, K.Y., and Shiu, K.K., Kinetics of o-benzoquinone mediated oxidation of glucose by glucose oxidase at edge plane pyrolytic graphite electrode, Electroanalysis, 1996, vol. 8, no. 6, p. 597.
  11. delle Noci, S., Frasconi, M., Favero, G., Tosi, M., Ferri, T., and Mazzei, F., Electrochemical kinetic characterization of redox mediated glucose oxidase reactions: A simplified approach, Electroanalysis, 2008, vol. 20, no. 2, p. 163.
  12. Limoges, B. and Savéant, J.M., Cyclic voltammetry of immobilized redox enzymes. Interference of steady-state and non-steady-state Michaelis–Menten kinetics of the enzyme–redox cosubstrate system, J. Electroanal. Chem., 2003, vol. 549, p. 61.
  13. Yokoyama, K. and Kayanuma, Y., Cyclic voltammetric simulation for electrochemically mediated enzyme reaction and determination of enzyme kinetic constants, Analytical Chem., 1998, vol. 70, no. 16, p. 3368.
  14. Herenda, S., Ostojić, J., Hasković, E., Hasković, D., Miloš, M., and Galić, B., Electrochemical investigation of the influence of K2[B3O3F4OH] on the activity of immobilized superoxide dismutase, Int. J. Electrochem. Sci., 2018, vol. 13, p. 3279.
  15. Britz, D. and Strutwolf, J., Digital simulation of chronoamperometry at an electrode within a hemispherical polymer drop containing an enzyme: Comparison of a hemispherical with a flat disk electrode, Biosens. Bioelectron., 2013, vol. 50, p. 269.
  16. Araminaitė, R., Garjonytė, R., and Malinauskas, A., Rotating disk electrode study of Prussian blue-and glucose oxidase-based bioelectrode, J. Electroanal. Chem., 2012, vol. 672, p. 12.
  17. Sekretaryova, A.N., Vagin, M.Y., Beni, V., Turner, A.P., and Karyakin, A.A., Unsubstituted phenothiazine as a superior water-insoluble mediator for oxidases, Biosens. Bioelectron., 2014, vol. 53, p. 275.
  18. Ikeda, T., Katasho, I., Kamei, M., and Senda, M., Electrocatalysis with a glucose-oxidase-immobilized graphite electrode, Agric. Biol. Chem., 1984, vol. 48, no. 8, p. 1969.
  19. Prévoteau, A., Geirnaert, A., Arends, J.B., Lannebère, S., Van de Wiele, T., and Rabaey, K., Hydrodynamic chronoamperometry for probing kinetics of anaerobic microbial metabolism–case study of Faecalibacterium prausnitzii, Sci. Rep., 2015, vol. 5, p. 11484.
  20. Léger, C., Dementin, S., Bertrand, P., Rousset, M., and Guigliarelli, B., Inhibition and aerobic inactivation kinetics of Desulfovibrio fructosovorans NiFe hydrogenase studied by protein film voltammetry, J. Amer. Chem. Soc., 2004, vol. 126, no. 38, p. 12162.
  21. Dmitrieva, M.V., Zolotukhina, E.V., Gerasimova, E.V., Terent’ev, A.A., and Dobrovol’skii, Y.A., Dehydrogenase and electrochemical activity of Escherichia coli extracts, Appl. Biochem. Microbiol., 2017, vol. 53, p. 458.
  22. Dmitrieva, M.V., Gerasimova, E.V., Terent’ev, A.A., Dobrovol’skii, Y.A., and Zolotukhina, E.V., Electrochemical peculiarities of mediator-assisted bioelectrocatalytic oxidation of glucose by a new type of bioelectrocatalyst, Russ. J. Electrochem., 2019, vol. 55, p. 889.
  23. Zolotukhina, E.V., Chaika, M.Yu., Kravchenko, T.A., Novikova, V.V., Bulavina, E.V., and Vdovina, S.N., Electronic conductivity and potential of sulfocation-exchange membrane MK-40 modified by disperse copper, Sorbtsionnye Khromatogr. Protsessy, 2008, vol. 8, no. 4, p. 636.
  24. Kegg: Metabolic pathways—Escherichia coli O25b:K100:H4-ST131 EC958 (UPEC)
  25. Han, M.-J. and Lee, S.Y., The Escherichia coli proteome: past, present and future prospects, Microbiol. Mol. Biol. Rev., 2006, vol. 70, no. 2, p. 362.
  26. Ghaly, A.E. and Mahmoud, N.S., Optimum conditions for measuring dehydrogenase activity of Aspergillus niger using TTC, Amer. J. Biochem. and Biotechnol., 2006, vol. 2, no. 4, p. 186.
  27. https://www.brenda-enzymes.org/enzyme.php?ecno=
  28. Shijie, Liu, Bioprocess Engineering: Kinetics, Sustainability, and Reactor Design, Amsterdam: Elsevier, 2016.
  29. Reed, M.C., Lieb, A., and Nijhout, H.F., The biological significance of substrate inhibition: a mechanism with diverse functions, Bioessays, 2010, vol.32, no. 5, p.422.
  30. Doran, P M., Bioprocess Engineering Principles, London: Acad. Press Limited, 1995.
  31. Mehdinia, A., Ehsan, Z., and Jabbari, A., Facile microwave-assisted synthesized reduced graphene oxide/tin oxide nanocomposite and using as anode material of microbial fuel cell to improve power generation, Int. J. Hydrogen Energy, 2014, vol. 39, no. 20, p. 10724.
  32. Miyake, T., Haneda, K., Nagai, N., Yatagawa, Y., Onami, H., Yoshino, S., and Nishizawa, M., Enzymatic biofuel cells designed for direct power generation from biofluids in living organisms, Energy Environ. Sci., 2011, vol. 4, no. 12, p. 5008.
  33. Gonzalez-Solino, C. and Lorenzo, M.D., Enzymatic fuel cells: Towards self-powered implantable and wearable diagnostics, Biosensors, 2018, vol. 8, no. 1, p. 11.