High-valent metal-oxo intermediates in energy demanding processes: from dioxygen reduction to water splitting
Graphical abstract
Introduction
The demand for fuel cell technology has increased sharply over the last three decades, as development has been driven by a growing awareness of issues related to anthropogenic climate change and an increase in global energy demand [1]. The most commonly used hydrogen fuel cell involves the oxidation of hydrogen to protons at a platinum anode and the four-electron reduction of O2 to water at the cathode by Pt impregnated in carbon. The high loadings of this precious metal that are required to achieve appreciable activity have prompted the development of H2 oxidation [2] and O2 reduction catalysts [3] based on nonprecious metals. Furthermore, owing to issues of compression and storage, research has been on-going into alternative ‘hydrogen-storage’ compounds [4], that can guarantee similar performance in a more convenient form. Water is the ultimate candidate as a source for hydrogen underpinning the intense interest in creating artificial systems that use catalysts based on earth abundant elements to achieve the splitting of water into hydrogen and oxygen and their recombination to obtain clean energy in a closed-cycle fuel cell [5, 6, 7]. The oxidation of H2O to O2 is a four-electron, four-proton process in which OO bond formation is the key chemical step [8, 9, 10, 11]. In photosystem II, these proton-coupled electron transfer (PCET) reactions occur via a tyrosine that is in close proximity to the Mn4Ca oxygen-evolving complex. Similarly, a range of other metalloenzymes achieve the challenging tasks of dioxygen reduction [12, 13, 14, 15, 16] and hydrogen production [17, 18] to fulfill the function of energy supply systems in biology by using cheap and non-toxic metals under ambient conditions of pressure and temperature. However, the large size and relative instability under aerobic conditions of many of these enzymes, and the difficulties associated with their purification process, has led to the search for well-defined molecular complexes for O2 reduction, water oxidation and hydrogen production.
Advances in our understanding of the mechanism of biological systems may allow vital insights into the prerequisites necessary for the design of efficient catalysts for O2 reduction and water oxidation by using cheap and readily available first row transition-metals under ambient conditions. High-valent metal-oxo cores have been proposed, and in few cases isolated, as the common reactive intermediates in these biological reactions relevant to renewable energy formation (Figure 1), thereby making them attractive targets for biomimetic synthetic studies. Recent synthetic advances have led to the isolation and characterization of several well-described metal-oxo model complexes, and detailed reactivity studies in conjunction with spectroscopy and theory have helped to understand how the steric and electronic properties of the metal centers modulate their reactivity [19, 20, 21, 22, 23, 24, 25, 26, 27]. Although the synthetic metal-oxo complexes have been found to be reactive toward substrates containing weak CH bonds, in most cases the exhibited reactions are moderate and non-catalytic, with activities falling far short of the activity of the biological catalysts. Moreover, only in extremely rare cases they are found to be efficient in initiating OO bond formation reactions. Similarly, evidences for the involvement of metal-oxo cores in artificial systems that perform catalytic dioxygen reduction have only been obtained in a limited number of cases.
In this review, we summarize some of the recent advances in bioinorganic chemistry that strengthen the proposed involvement of metal-oxo cores in transition metal mediated transformations related to energy conversion and conservation processes. In our discussion we focus on the sparse literature existing on the detailed mechanistic studies of bio-relevant transition metal complexes, where the involvement of metal-oxo cores as active intermediates has been conclusively evidenced based on spectroscopic and kinetic studies during biomimetic dioxygen reduction and water oxidation reactions.
Section snippets
Nucleophilic versus electrophilic oxo
It is important to understand the electronic structure of the metal-oxo unit in order to rationalize the diversity of redox processes it can perform in biology. Gray and others [29] have shown that the oxo ligand in mono-oxo complexes with d0–d2 electron configurations in a tetragonal environment, is considered to be electrophilic because of π bonding between the oxygen lone pairs and the d(xz) and d(yz) orbitals on the metal center (Figure 1a). In d2 complexes, the two d-electrons occupy the d(
Dioxygen reduction
Cytochrome c oxidase (CcO) and related heme/copper terminal oxidases are the fuel cells of aerobic organisms. These enzymes catalyze the selective and complete four-proton, four-electron conversion of dioxygen to water without releasing partially reduced peroxide (or superoxide) intermediates that are toxic to cells [13, 15, 16, 33]. CcO is distinguished structurally from other heme-dependent proteins of O2 metabolism, owing to the presence of an essential copper metal center proximate to the
Conclusion
The production of hydrogen and oxygen from water and sunlight represents an attractive means of artificial energy conversion for a world still largely dependent on fossil fuels. A practical technology for producing solar-derived fuels remains an unachieved goal, however, and is dependent on developing a better understanding of the key step, the OO bond formation reaction leading to the oxidation of water to dioxygen. Similarly, OO cleavage leading to the four-electron reduction of dioxygen is
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
The authors gratefully acknowledge research support of this work by the NRF of Korea through CRI (NRF-2012R1A3A2048842 to WN) and GRL (NRF-2010-00353 to WN), the German funding agency Deutsche Forschungsgemeinschaft (Cluster of Excellence ‘Unifying Concepts in Catalysis’, grant number EXC 314/1 to KR) and Cost Action (CM1305 ECOSTBio to KR).
References (83)
- et al.
Design principles of proton-pumping haem–copper oxidases
Curr Opin Struct Biol
(2006) - et al.
Intermediates generated during the reaction of reduced Rhodobacter sphaeroides cytochrome c oxidase with dioxygen
BBA — Bioenergetics
(2013) - et al.
The origin of the FeIVO intermediates in cytochrome aa3 oxidase
BBA — Bioenergetics
(2012) - et al.
[NiFe] hydrogenases: a common active site for hydrogen metabolism under diverse conditions
BBA — Bioenergetics
(2013) - et al.
Intrinsic properties and reactivities of mononuclear nonheme iron–oxygen complexes bearing the tetramethylcyclam ligand
Coord Chem Rev
(2013) Electron-transfer properties of high-valent metal-oxo complexes
Coord Chem Rev
(2013)- et al.
Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase
Science
(1998) - et al.
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
Nature
(2011) - et al.
A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II
Science
(2011) - et al.
Powering the planet: chemical challenges in solar energy utilization
Proc Natl Acad Sci U S A
(2006)
A molecular molybdenum-oxo catalyst for generating hydrogen from water
Nature
A review on non-precious metal electrocatalysts for PEM fuel cells
Energy Environ Sci
Carbon-free energy: a review of ammonia- and hydrazine-based electrochemical fuel cells
Energy Environ Sci
Structure and function of photosynthetic reaction centres
Molecular Solar Fuels
Artificial photosynthesis: molecular systems for catalytic water oxidation
Chem Rev
Progress in base-metal water oxidation catalysis
ChemSusChem
Photosystem II: the light-driven water: plastoquinone oxidoreductase
Biological water oxidation
Acc Chem Res
Water-splitting chemistry of photosystem II
Chem Rev
The mechanism of water oxidation: from electrolysis via homogeneous to biological catalysis
ChemCatChem
Copper oxygen chemistry
Heme/copper terminal oxidases
Chem Rev
Hydrogenases
Chem Rev
Status of reactive non-heme metal-oxygen intermediates in chemical and enzymatic reactions
J Am Chem Soc
The biology and chemistry of high-valent iron-oxo and iron-nitrido complexes
Nat Commun
Terminal oxo and imido transition-metal complexes of groups 9–11
Eur J Inorg Chem
Tuning reactivity and mechanism in oxidation reactions by mononuclear nonheme iron(IV)-oxo complexes
Acc Chem Res
Dioxygen activation by metalloenzymes and models
Acc Chem Res
Role of metal-oxo complexes in the cleavage of CH bonds
Chem Soc Rev
CH bond activations by metal oxo compounds
Chem Rev
Direct observation of intermediates formed during steady-state electrocatalytic O2 reduction by iron porphyrins
Proc Natl Acad Sci U S A
Electronic structures of oxo-metal ions
The electronic nature of terminal oxo ligands in transition-metal complexes: ambiphilic reactivity of oxorhenium species
J Am Chem Soc
Electronic design criteria for OO bond formation via metal-oxo complexes
Inorg Chem
Nonheme oxo-iron(IV) intermediates form an oxyl radical upon approaching the CH bond activation transition state
Proc Natl Acad Sci U S A
Active site intermediates in the reduction of O2 by cytochrome oxidase, and their derivatives
BBA — Bioenergetics
Mass spectrometric determination of dioxygen bond splitting in the “peroxy” intermediate of cytochrome c oxidase
Proc Natl Acad Sci U S A
Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase
Proc Natl Acad Sci U S A
Recent applications of a synthetic model of cytochrome c oxidase: beyond functional modeling
Inorg Chem
Synthetic models for heme–copper oxidases
Chem Rev
Heme–copper/dioxygen adduct formation properties, and reactivity
Acc Chem Res
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