Electric Field Induced Biomimetic Transmembrane Electron Transport using Carbon Nanotube Porins as Bipolar Electrodes

<p>Cells modulate their homeostasis through the control of redox reactions via transmembrane electron transport systems. These are largely mediated via oxidoreductase enzymes. Their use in biology has been linked to a host of systems including reprogramming for energy requirements in cancer. Consequently, our ability to modulate membrane redox systems may give rise to opportunities to modulate underlying biology. The current work aimed to develop a wireless bipolar electrochemical approach to form on-demand electron transfer across biological membranes. To achieve this goal, we show that using membrane inserted carbon nanotube porins that can act as bipolar nanoelectrodes, we could control electron flow with externally applied electric fields across membranes. Before this work, bipolar electrochemistry has been thought to require high applied voltages not compatible with biological systems. We show that bipolar electrochemical reaction via gold reduction at the nanotubes could be modulated at low cell-friendly voltages, providing an opportunity to use bipolar electrodes to control electron flux across membranes. Our observations present a new opportunity to use bipolar electrodes to alter cell behavior via wireless control of membrane electron transfer.</p>

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Electric Field Induced Biomimetic Transmembrane Electron Transport using Carbon Nanotube Porins as Bipolar Electrodes

10.26434/chemrxiv.14413457.v2 ◽

2021 ◽

Author(s):

Jacqueline M. Hicks ◽

Yun-Chiao Yao ◽

Sydney Barber ◽

Nigel Neate ◽

Julie Watts ◽

...

Keyword(s):

Electron Transfer ◽

Carbon Nanotube ◽

Electron Transport ◽

Electric Fields ◽

Electron Flow ◽

Transport Systems ◽

Redox Systems ◽

Bipolar Electrodes ◽

Electrochemical Approach ◽

Transmembrane Electron Transport

<p>Cells modulate their homeostasis through the control of redox reactions via transmembrane electron transport systems. These are largely mediated via oxidoreductase enzymes. Their use in biology has been linked to a host of systems including reprogramming for energy requirements in cancer. Consequently, our ability to modulate membrane redox systems may give rise to opportunities to modulate underlying biology. The current work aimed to develop a wireless bipolar electrochemical approach to form on-demand electron transfer across biological membranes. To achieve this goal, we show that using membrane inserted carbon nanotube porins that can act as bipolar nanoelectrodes, we could control electron flow with externally applied electric fields across membranes. Before this work, bipolar electrochemistry has been thought to require high applied voltages not compatible with biological systems. We show that bipolar electrochemical reaction via gold reduction at the nanotubes could be modulated at low cell-friendly voltages, providing an opportunity to use bipolar electrodes to control electron flux across membranes. Our observations present a new opportunity to use bipolar electrodes to alter cell behavior via wireless control of membrane electron transfer.</p>

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Electric Field Induced Biomimetic Transmembrane Electron Transport Using Carbon Nanotube Porins

Small ◽

10.1002/smll.202102517 ◽

2021 ◽

pp. 2102517

Author(s):

Jacqueline M. Hicks ◽

Yun‐Chiao Yao ◽

Sydney Barber ◽

Nigel Neate ◽

Julie A. Watts ◽

...

Keyword(s):

Carbon Nanotube ◽

Electron Transport ◽

Electric Field ◽

Transmembrane Electron Transport

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Tracking Electron Uptake from a Cathode into Shewanella Cells: Implications for Energy Acquisition from Solid-Substrate Electron Donors

mBio ◽

10.1128/mbio.02203-17 ◽

2018 ◽

Vol 9 (1) ◽

Cited By ~ 43

Author(s):

Annette R. Rowe ◽

Pournami Rajeev ◽

Abhiney Jain ◽

Sahand Pirbadian ◽

Akihiro Okamoto ◽

...

Keyword(s):

Electron Transfer ◽

Electron Transport ◽

Complex I ◽

Electron Transport Chain ◽

Electron Flow ◽

Extracellular Electron Transfer ◽

Terminal Electron Acceptor ◽

Cellular Energy ◽

Transport Chain ◽

Energy Acquisition

ABSTRACTWhile typically investigated as a microorganism capable of extracellular electron transfer to minerals or anodes,Shewanella oneidensisMR-1 can also facilitate electron flow from a cathode to terminal electron acceptors, such as fumarate or oxygen, thereby providing a model system for a process that has significant environmental and technological implications. This work demonstrates that cathodic electrons enter the electron transport chain ofS. oneidensiswhen oxygen is used as the terminal electron acceptor. The effect of electron transport chain inhibitors suggested that a proton gradient is generated during cathode oxidation, consistent with the higher cellular ATP levels measured in cathode-respiring cells than in controls. Cathode oxidation also correlated with an increase in the cellular redox (NADH/FMNH2) pool determined with a bioluminescence assay, a proton uncoupler, and a mutant of proton-pumping NADH oxidase complex I. This work suggested that the generation of NADH/FMNH2under cathodic conditions was linked to reverse electron flow mediated by complex I. A decrease in cathodic electron uptake was observed in various mutant strains, including those lacking the extracellular electron transfer components necessary for anodic-current generation. While no cell growth was observed under these conditions, here we show that cathode oxidation is linked to cellular energy acquisition, resulting in a quantifiable reduction in the cellular decay rate. This work highlights a potential mechanism for cell survival and/or persistence on cathodes, which might extend to environments where growth and division are severely limited.IMPORTANCEThe majority of our knowledge of the physiology of extracellular electron transfer derives from studies of electrons moving to the exterior of the cell. The physiological mechanisms and/or consequences of the reverse processes are largely uncharacterized. This report demonstrates that when coupled to oxygen reduction, electrode oxidation can result in cellular energy acquisition. This respiratory process has potentially important implications for how microorganisms persist in energy-limited environments, such as reduced sediments under changing redox conditions. From an applied perspective, this work has important implications for microbially catalyzed processes on electrodes, particularly with regard to understanding models of cellular conversion of electrons from cathodes to microbially synthesized products.

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Reactions of electron-transfer proteins at electrodes

Quarterly Reviews of Biophysics ◽

10.1017/s0033583500000366 ◽

1985 ◽

Vol 18 (3) ◽

pp. 261-322 ◽

Cited By ~ 114

Author(s):

Fraser A. Armstrong ◽

H. Allen O. Hill ◽

Nicholas J. Walton

Keyword(s):

Electron Transfer ◽

Electron Transport ◽

Protein Interactions ◽

Dynamic Properties ◽

Three Dimensional ◽

Structural Data ◽

Transport Systems ◽

Electrode Surfaces ◽

Electron Transfer Proteins ◽

Redox Sites

Studies of electron-transfer reactions of redox proteins have, in recent years, attracted widespread interest and attention. Progress has been evident from both physical and biological standpoints, with the increasing availability of three-dimensional structural data for many small electron-transfer proteins prompting a variety of systematic investigations (Isied, 1985). Most recently, attention has been directed towards questions concerning the elementary transfer of electrons between spatially remote redox sites, and the nature of protein–protein interactions which, for intermolecular processes, stabilize specific precursor complexes which may be optimally juxtaposed for electron-transfer. These and other issues, including the necessary reversibility of protein interfacial interactions and the dynamic properties of proteins as carriers of electrons in biological electron-transport systems, are now being addressed in the rapidly emerging field of direct (unmediated) protein electrochemistry. It is our intention in this article to discuss developments made in this area and highlight points which we believe to have the most bearing on our current understanding of diffusion-dominated, protein-mediated electron transport at electrode surfaces. First we shall outline some basic considerations which are best considered with reference to homogeneous systems.

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ChemInform Abstract: ORGANIC ELECTRON TRANSPORT SYSTEMS. I. ELECTROCHEMICAL AND SPECTROSCOPIC STUDY OF BROMO-SUBSTITUTED TRIARYLAMINE REDOX SYSTEMS

Chemischer Informationsdienst ◽

10.1002/chin.198018072 ◽

1980 ◽

Vol 11 (18) ◽

Author(s):

W. SCHMIDT ◽

E. STECKHAN

Keyword(s):

Electron Transport ◽

Spectroscopic Study ◽

Transport Systems ◽

Redox Systems ◽

Organic Electron

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Tracking electron uptake from a cathode intoShewanellacells: implications for generating maintenance energy from solid substrates

10.1101/116475 ◽

2017 ◽

Cited By ~ 2

Author(s):

Annette R. Rowe ◽

Pournami Rajeev ◽

Abhiney Jain ◽

Sahand Pirbadian ◽

Akihiro Okamotao ◽

...

Keyword(s):

Electron Transfer ◽

Electron Transport ◽

Electron Transport Chain ◽

Nadh Oxidase ◽

Electron Flow ◽

Proton Pumping ◽

Model Systems ◽

Extracellular Electron Transfer ◽

Terminal Electron Acceptor ◽

Transport Chain

While typically investigated as a microorganism capable of extracellular electron transfer to minerals or anodes,Shewanella oneidensisMR-1 can also facilitate electron flow from a cathode to terminal electron acceptors such as fumarate or oxygen, thereby providing a model systems for a process that has significant environmental and technological implications. This work demonstrates that cathodic electrons enter the electron transport chain of S.oneidensiswhen oxygen is used as the terminal electron acceptor. The effect of electron transport chain inhibitors suggested that a proton gradient is generated during cathode-oxidation, consistent with the higher cellular ATP levels measured in cathode-respiring cells relative to controls. Cathode oxidation also correlated with an increase in the cellular redox (NADH/FMNH2) pool using a bioluminescent assay. Using a proton uncoupler, generation of NADH/FMNH2under cathodic conditions was linked to reverse electron flow mediated by the proton pumping NADH oxidase Complex I. A decrease in cathodic electron uptake was observed in various mutant strains including those lacking the extracellular electron transfer components necessary for anodic current generation. While no cell growth was observed under these conditions, here we show that cathode oxidation is linked to cellular energy conservation, resulting in a quantifiable reduction in cellular decay rate. This work highlights a potential mechanism for cell survival and/or persistence in environments where growth and division are severely limited.

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