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Reconstitution of supramolecular organization involved in energy metabolism at electrochemical interfaces for biosensing and bioenergy production

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Abstract

How the redox proteins and enzymes involved in bioenergetic pathways are organized is a relevant fundamental question, but our understanding of this is still incomplete. This review provides a critical examination of the electrochemical tools developed in recent years to obtain knowledge of the intramolecular and intermolecular electron transfer processes involved in metabolic pathways. Furthermore, better understanding of the electron transfer processes associated with energy metabolism will provide the basis for the rational design of biotechnological devices such as electrochemical biosensors, enzymatic and microbial fuel cells, and hydrogen production factories. Starting from the redox complexes involved in two relevant bacterial chains, i.e., from the hyperthermophile Aquifex aeolicus and the acidophile Acidithiobacillus ferrooxidans, examination of protein–protein interactions using electrochemistry is first reviewed, with a focus on the orientation of a protein on an electrochemical interface mimic of a physiological interaction between two partners. Special attention is paid to current research in the electrochemistry of essential membrane proteins, which is one mandatory step toward the understanding of energy metabolic pathways. The complex and challenging architectures built to reconstitute a membrane-like environment at an electrode are especially considered. The role played by electrochemistry in the attempt to consider full bacterial metabolism is finally emphasized through the study of whole cells immobilized at electrodes as suspensions or biofilms. Before the performances of biotechnological devices can be further improved to make them really attractive, questions remain to be addressed in this particular field of research. We discuss the bottlenecks that need to be overcome in the future.

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Abbreviations

CcO:

Cytochrome c oxidase

DET:

Direct electron transfer

DvH:

Desulfovibrio vulgaris Hildenborough

PMIRRAS:

Polarization-modulation infrared reflection–adsorption spectroscopy

QCM:

Quartz crystal microbalance

SAM:

Self-assembled monolayer

SEIRA:

Surface-enhanced infrared absorption

SHE:

Standard hydrogen electrode

t-BLM:

Tethered bilayer lipid membrane

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Acknowledgments

The authors thank Région Provence-Alpes-Côte d’Azur, CNRS, and ANR Bioénergie no. ANR-2010-BIOE-003-01 for financial support.

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Authors and Affiliations

  1. Unité de Bioénergétique et Ingénierie des Protéines, UMR7281-FR3479, Centre National de la Recherche Scientifique, Aix Marseille Université, 31 chemin Joseph Aiguier, 13009, Marseille, France

    M. Roger, A. de Poulpiquet, A. Ciaccafava, M. Ilbert, M. Guiral, M. T. Giudici-Orticoni & E. Lojou

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  1. M. Roger
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  2. A. de Poulpiquet
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  3. A. Ciaccafava
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  4. M. Ilbert
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  5. M. Guiral
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  6. M. T. Giudici-Orticoni
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  7. E. Lojou
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Correspondence to E. Lojou.

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Published in the special issue Analytical Science in France with guest editors Christian Rolando and Philippe Garrigues.

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Roger, M., de Poulpiquet, A., Ciaccafava, A. et al. Reconstitution of supramolecular organization involved in energy metabolism at electrochemical interfaces for biosensing and bioenergy production. Anal Bioanal Chem 406, 1011–1027 (2014). https://doi.org/10.1007/s00216-013-7465-1

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