Redox cofactor from biological energy transduction as molecularly tunable energy-storage compound.

Abstract

Energy transduction and storage in biological systems involve multiply coupled, stepwise reduction/oxidation of energycarrying molecules such as adenosine triphosphate (ATP), nicotinamide, and flavin cofactors. These are synthesized as a result of oxidation during citric acid cycles in mitochondria or during photosynthesis in chloroplasts, and high energies stored in their chemical bonds are consequently harnessed for many biological reactions. Phosphorylation and protonation are key underlying mechanisms that allow for reversible cycling and regulate the molecule-specific redox potential. A sequential progression of electron transfer through the redox cascades as well as continuous recycling of the redox centers enables efficient energy use in biological systems. The biological energy transductionmechanism hints at the construction of a man-made energy storage system. Since the pioneering work by Tarascon and co-workers towards a sustainable lithium rechargeable battery received significant resonance, organic materials such as carbonyl, carboxy, or quinone-based compounds have been demonstrated to be bio-inspired organic electrodes. The imitation of redoxactive plastoquinone and ubiquinone cofactors through the use of redox-active C=O functionalities in organic electrodes is a significant step forward to biomimetic energy storage. However, the biological energy transduction is based on numerous redox centers of versatile functionalities available in nature, not limited to the simple redox active C=O functionalities. Consideration of how natural energy transduction systems function at organelle or cellular levels by elucidating the basic components and their operating principles selected by evolution will enrich the biomimetic strategy for efficient and green energy storage. Flavins are one of most structurally and functionally versatile redox centers in nature, catalyzing an enormous range of biotransformations and electron-transfer reactions, which occur over a wide potential range (> 500 mV). The extraordinary versatility of flavins stems from their ability to engage in either oneor twoelectron-transfer redox processes, accompanying proton transfer at the nitrogen atoms of diazabutadiene motif. In the respiratory electron transport chain, for example, electrons from reduced flavin adenine dinucleotide (FADH2) are transported along a group of proteins located in the inner membrane of mitochondria to induce proton pumping across the membrane, as illustrated in Figure 1a (left). This process generates an electrochemical proton gradient, which results in the formation of high-energy ATP. FAD is reduced again in the citric acid cycle of mitochondria, which enables continuous recycling of flavin redox centers. A close analogy exists between the key components, facilitating respiration and battery operation (Figure 1a); charged ions (H or Li) and electrons, which are derived from flavin redox centers, are unidirectionally transported in a stoichiometric manner using separated paths. This creates chemical gradients across membranes, and finally results in the formation of highenergy species such as ATP and metallic lithium. Herein, we report on the possibility of using the energystorage mechanism of flavin redox cycling in mitochondria to lithium rechargeable batteries. According to our results, flavin electrodes were capable of reversibly storing and releasing two lithium ions and two electrons per formula unit. Redox reactions in flavin electrodes were thoroughly investigated using the combined analyses of ex situ characterizations and density functional theory (DFT)-based calculations. We found that the flavin redox reaction occurs during battery operation at the nitrogen atoms of the diazabutadiene motif in flavin molecules using two successive single-electron transfer steps, in a similar way to the proton-coupled electron transfer in flavoenzymes. Molecular tuning by chemical substitution on the isoalloxazine ring significantly improved electrochemical performances in terms of an average redox potential, a gravimetric capacity, and stability, resulting in a high-energy density comparable to that of LiFePO4, the [*] M. Lee, D. H. Nam, Prof. C. B. Park Department of Materials Science and Engineering Korea Advanced Institute of Science and Technology Daejeon 305-701 (Korea) E-mail: parkcb@kaist.ac.kr J. Hong, Dr. D.-H. Seo, Prof. K. T. Nam, Prof. K. Kang Center for Nanoparticle Research Institute for Basic Science (IBS) Department of Materials Science and Engineering Research Institute of Advanced Materials Seoul National University, Seoul 151-742 (Korea) E-mail: matlgen1@snu.ac.kr [] These authors contributed equally to this work.

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Identifiers

DOI

10.1002/anie.201301850

Journal

Angewandte Chemie International Edition

Year

2013