Mediatorless Direct Electron Transfer between Flavin Adenine Dinucleotide-Dependent Glucose Dehydrogenase and Single-Walled Carbon Nanotubes

Hitoshi Muguruma, Hisanori Iwasa, Hiroki Hidaka, Atsunori Hiratsuka, Hirotaka Uzawa

Research output: Contribution to journalArticle

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Abstract

The flavoenzymes flavin adenine dinucleotide-dependent glucose dehydrogenase (FAD-GDH) and oxidase (FAD-GOx) do not undergo direct electron transfer (DET) at conventional electrodes, because the flavin adenine dinucleotide (FAD) cofactor is buried deeply (∼1.4 nm) below the protein surface. We present a mediator-less DET between oxygen-insensitive FAD-GDH and single-walled carbon nanotubes (SWCNTs). A glucose-concentration-dependent current (GCDC) is observed at the electrode with the combination of glycosylated FAD-GDH and debundled SWCNTs; the GCDC, because of an increase in the polarized potential during potential sweep voltammetry, increases steeply (+0.1 V of onset, 1.2 mA cm-2 at +0.6 V 48 mM glucose) without the appearance of the FAD redox peak at -0.45 V. In the control experiment, the GCDC is not observed at the counterpart with either bundled SWCNTs or debundled multiwalled carbon nanotubes (MWCNTs). In the control experiment, the GCDC is observed at an analogous electrode based on oxygen-sensitive FAD-GOx with all CNT types (bundled SWCNTs, debundled SWCNTs, and debundled MWCNTs) in the presence of oxygen because oxygen acts as a natural and mobile mediator. Therefore, observation of the GCDC at the electrode with oxygen-insensitive FAD-GDH and debundled SWCNTs provides evidence of mediator-less DET, even though oxygen is present. Details of the DET are discussed with respect to the recently reported crystallographic model of FAD-GDH. The three-dimensional globular FAD-GDH molecule is 4.5 nm × 5.6 nm × 7.8 nm, which is larger than the 1.2 nm diameter of an individual SWCNT and smaller than the 10 nm diameter of an individual MWCNT and the 1 μm size of a SWCNT bundle. Only individual SWCNTs can be plugged into the groove of FAD-GDH, which is close to and within 1.0 nm of FAD, while maintaining their catalytic activity. Images obtained using transmission electron and atomic force microscopies support the stated configuration of FAD-GDH molecules and debundled SWCNTs. We demonstrate that DET can be explained by quantum tunneling theory. Electrochemical experiments with various FAD-GDHs suggest that (i) DET with debundling SWCNT can be applied to any type of FAD-GDH, (ii) the electrode with various types of FAD-GDH implements superior functions (compared to an analogous electrode with FAD-GOx and nicotineamide adenine dinucleotide-GDH), and (iii) glycan chains present on FAD-GDH prevent denaturation when the SWCNT is close to FAD.

LanguageEnglish
Pages725-734
Number of pages10
JournalACS Catalysis
Volume7
Issue number1
DOIs
StatePublished - 2017 Jan 6

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Glucose 1-Dehydrogenase
Flavin-Adenine Dinucleotide
Single-walled carbon nanotubes (SWCN)
Glucose
Electrons
Oxygen
Electrodes
Multiwalled carbon nanotubes (MWCN)
Oxidoreductases

Keywords

  • biosensor
  • debundling
  • direct electron transfer
  • flavin adenine dinucleotide-dependent glucose dehydrogenase
  • single-walled carbon nanotube

ASJC Scopus subject areas

  • Catalysis

Cite this

Mediatorless Direct Electron Transfer between Flavin Adenine Dinucleotide-Dependent Glucose Dehydrogenase and Single-Walled Carbon Nanotubes. / Muguruma, Hitoshi; Iwasa, Hisanori; Hidaka, Hiroki; Hiratsuka, Atsunori; Uzawa, Hirotaka.

In: ACS Catalysis, Vol. 7, No. 1, 06.01.2017, p. 725-734.

Research output: Contribution to journalArticle

Muguruma, Hitoshi ; Iwasa, Hisanori ; Hidaka, Hiroki ; Hiratsuka, Atsunori ; Uzawa, Hirotaka. / Mediatorless Direct Electron Transfer between Flavin Adenine Dinucleotide-Dependent Glucose Dehydrogenase and Single-Walled Carbon Nanotubes. In: ACS Catalysis. 2017 ; Vol. 7, No. 1. pp. 725-734
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N2 - The flavoenzymes flavin adenine dinucleotide-dependent glucose dehydrogenase (FAD-GDH) and oxidase (FAD-GOx) do not undergo direct electron transfer (DET) at conventional electrodes, because the flavin adenine dinucleotide (FAD) cofactor is buried deeply (∼1.4 nm) below the protein surface. We present a mediator-less DET between oxygen-insensitive FAD-GDH and single-walled carbon nanotubes (SWCNTs). A glucose-concentration-dependent current (GCDC) is observed at the electrode with the combination of glycosylated FAD-GDH and debundled SWCNTs; the GCDC, because of an increase in the polarized potential during potential sweep voltammetry, increases steeply (+0.1 V of onset, 1.2 mA cm-2 at +0.6 V 48 mM glucose) without the appearance of the FAD redox peak at -0.45 V. In the control experiment, the GCDC is not observed at the counterpart with either bundled SWCNTs or debundled multiwalled carbon nanotubes (MWCNTs). In the control experiment, the GCDC is observed at an analogous electrode based on oxygen-sensitive FAD-GOx with all CNT types (bundled SWCNTs, debundled SWCNTs, and debundled MWCNTs) in the presence of oxygen because oxygen acts as a natural and mobile mediator. Therefore, observation of the GCDC at the electrode with oxygen-insensitive FAD-GDH and debundled SWCNTs provides evidence of mediator-less DET, even though oxygen is present. Details of the DET are discussed with respect to the recently reported crystallographic model of FAD-GDH. The three-dimensional globular FAD-GDH molecule is 4.5 nm × 5.6 nm × 7.8 nm, which is larger than the 1.2 nm diameter of an individual SWCNT and smaller than the 10 nm diameter of an individual MWCNT and the 1 μm size of a SWCNT bundle. Only individual SWCNTs can be plugged into the groove of FAD-GDH, which is close to and within 1.0 nm of FAD, while maintaining their catalytic activity. Images obtained using transmission electron and atomic force microscopies support the stated configuration of FAD-GDH molecules and debundled SWCNTs. We demonstrate that DET can be explained by quantum tunneling theory. Electrochemical experiments with various FAD-GDHs suggest that (i) DET with debundling SWCNT can be applied to any type of FAD-GDH, (ii) the electrode with various types of FAD-GDH implements superior functions (compared to an analogous electrode with FAD-GOx and nicotineamide adenine dinucleotide-GDH), and (iii) glycan chains present on FAD-GDH prevent denaturation when the SWCNT is close to FAD.

AB - The flavoenzymes flavin adenine dinucleotide-dependent glucose dehydrogenase (FAD-GDH) and oxidase (FAD-GOx) do not undergo direct electron transfer (DET) at conventional electrodes, because the flavin adenine dinucleotide (FAD) cofactor is buried deeply (∼1.4 nm) below the protein surface. We present a mediator-less DET between oxygen-insensitive FAD-GDH and single-walled carbon nanotubes (SWCNTs). A glucose-concentration-dependent current (GCDC) is observed at the electrode with the combination of glycosylated FAD-GDH and debundled SWCNTs; the GCDC, because of an increase in the polarized potential during potential sweep voltammetry, increases steeply (+0.1 V of onset, 1.2 mA cm-2 at +0.6 V 48 mM glucose) without the appearance of the FAD redox peak at -0.45 V. In the control experiment, the GCDC is not observed at the counterpart with either bundled SWCNTs or debundled multiwalled carbon nanotubes (MWCNTs). In the control experiment, the GCDC is observed at an analogous electrode based on oxygen-sensitive FAD-GOx with all CNT types (bundled SWCNTs, debundled SWCNTs, and debundled MWCNTs) in the presence of oxygen because oxygen acts as a natural and mobile mediator. Therefore, observation of the GCDC at the electrode with oxygen-insensitive FAD-GDH and debundled SWCNTs provides evidence of mediator-less DET, even though oxygen is present. Details of the DET are discussed with respect to the recently reported crystallographic model of FAD-GDH. The three-dimensional globular FAD-GDH molecule is 4.5 nm × 5.6 nm × 7.8 nm, which is larger than the 1.2 nm diameter of an individual SWCNT and smaller than the 10 nm diameter of an individual MWCNT and the 1 μm size of a SWCNT bundle. Only individual SWCNTs can be plugged into the groove of FAD-GDH, which is close to and within 1.0 nm of FAD, while maintaining their catalytic activity. Images obtained using transmission electron and atomic force microscopies support the stated configuration of FAD-GDH molecules and debundled SWCNTs. We demonstrate that DET can be explained by quantum tunneling theory. Electrochemical experiments with various FAD-GDHs suggest that (i) DET with debundling SWCNT can be applied to any type of FAD-GDH, (ii) the electrode with various types of FAD-GDH implements superior functions (compared to an analogous electrode with FAD-GOx and nicotineamide adenine dinucleotide-GDH), and (iii) glycan chains present on FAD-GDH prevent denaturation when the SWCNT is close to FAD.

KW - biosensor

KW - debundling

KW - direct electron transfer

KW - flavin adenine dinucleotide-dependent glucose dehydrogenase

KW - single-walled carbon nanotube

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