Review ArticleArtificial water-soluble systems inspired by [FeFe]-hydrogenases for electro- and photocatalytic hydrogen production
Introduction
Hydrogen has been long regarded as an ideal post-oil energy carrier due to its environmental neutrality, high gravimetric energy density (e.g. 142 MJ kg−1), and ability to be stored in large quantities [[1], [2], [3], [4], [5]]. Hydrogenases utilizing earth-abundant metals, either Fe or Ni and Fe, to catalyze the reversible hydrogen production and uptake, are the most active molecular catalysts [6,7]. Out of the three types of enzymes, namely, [FeFe]-, [NiFe]- and [Fe]-hydrogenases [8,9], [FeFe]-hydrogenase attracted much attention owing to its astonishing turnover frequency (TOF) of up to 6000–9000 s−1 for H2 production under low overpotential [10]. The active site of [FeFe]-hydrogenases (the so-called H-cluster), at which the catalytic reaction takes place, consists of a unique [2Fe] sub-cluster covalently bound to a canonical [4Fe-4S] cluster via the thiolate of a cysteine residue (Scheme 1) [[11], [12], [13]]. In the active site, the two Fe atoms in the [2Fe] subunit, which are referred to as proximal (Fep) and distal (Fed) iron relative to the [4Fe-4S] cluster, are bridged via a 2-aza-propane (1,3)-dithiolate (adt) ligand [[14], [15], [16]], and are ligated by the strong field, small inorganic ligands such as CO and CN−, keeping the coordinated iron in low-spin state [17]. In contrast to the six-coordinated Fep atom, the distal iron is five-coordinated leaving an open coordination site where the H2 production and oxidation take place [18]. The bridging CO [19] ligand makes Fed atom to adopt a "rotated state" [20], which can stabilize the open coordination site at Fed, being responsible for the high activity of the enzyme [21]. Note that the bridging CO can also be terminal depending on the redox state of H-cluster [22]. The electrons involved in the redox reaction of 2H+ + 2e– ↔ H2 are accommodated by the changing oxidation states of the two redox active [2Fe] and [4Fe-4S] sub-clusters [23], while the protons are shuttled to the active site through the secondary amine moiety of the adt ligand and the connected proton channel provided by the surrounding protein matrix [18,24].
The butterfly [2Fe] subunit in H-cluster, which is synthetically accessible and feasibly modified either by exchange of the organic moiety in the bridging μ-dithiolate ligands or by replacement of the CO and/or CN− ligands on the central metals by typical inorganic coordination ligands [21,25], encourages the rising of organometallic chemistry of bioinspired diiron compounds featuring the formula of [(μ-SR)2{Fe(CO)3–nLn}2]. To date, over 1500 small-molecule diiron mimetics have been designed and prepared as candidates for the structural and functional investigations of the active site of [FeFe]-hydrogenases [[26], [27], [28], [29], [30], [31], [32], [33], [34], [35], [36], [37], [38], [39], [40], [41], [42], [43], [44], [45], [46], [47], [48], [49], [50]]. Note that most of the synthetic diiron mimetics are only soluble in organic solvents, while the water solubility, at least to a certain extent, is deemed critical for hydrogen evolving catalysts [51]. First, water ultimately serves as either the solvent or the proton source for H2 production under enzymatic conditions. Second, the catalysts suffer from large overpotentials, low catalytic rates and are often unstable during catalysis in non-aqueous solutions. Moreover, the ultimate goal in energy research is to combine water-splitting systems with H2 production. Therefore, the lack of solubility in water represents one of the main drawbacks of most present [FeFe]-hydrogenase active site mimetics. The development of a system capable of simulating the functionality of [FeFe]-hydrogenases via either electro- or photochemical pattern in aqueous milieu becomes a particularly attractive objective to pursue.
From a synthetic point of view, the molecular modification of introducing hydrophilic substituents is accessible to address the water-solubility issue of the artificial diiron mimetics. However, the natural metalloenzyme is composed of abundant elements. It seems unlikely that the small-molecule diiron mimetics can achieve the enzyme-like H2 production activity and retain structural stability throughout the catalytic cycle of HERs when removed from the specialized, protected environment within the natural enzyme and exposed to water [52,53]. Simply mimicking the active site of [FeFe]-hydrogenases is not sufficient to achieve the desired HER reactivity, catalyst stability, and solvent compatibility. In addition, the multiple subgroups around the active site of [FeFe]-hydrogenases play an significant role in natural catalysis via controlling the substrate accessing and/or product cleaving, providing site isolation, enhancing charge and proton transfer [[54], [55], [56]]. Therefore, efforts to develop bioinspired artificial systems with sophisticatedly engineered outer coordination sphere around the non-natural active site will promote catalysis through increased water solubility, reactivity, selectivity, and stability. Reviewed herein is the development of a variety of approaches reported over the past two decades to construct the artificial systems inspired by [FeFe]-hydrogenases to impart water solubility to the inherently hydrophobic diiron mimetics, and improve the reactivity of target systems toward either electrocatalytic or photocatalytic HERs.
Section snippets
Diiron dithiolates with hydrophilic ligands
In 1999, Pickett and co-workers reported a dianionic compound [(μ-pdt) Fe2(CO)4(CN)2]2– (1, Scheme 2, pdt = propane-1,3-dithiolate) as stable and very soluble mimetic of H-cluster in water [57]. However, 1 neither reacted with nor electrocatalyzed the reduction of protons in aqueous solution over the pH range 4.0–8.4. In the interim there had been few further work examining the water-soluble HER catalysis by the cyanide-containing diiron compounds (e.g. 2, Scheme 2) [58]. Instead, the
Diiron dithiolates incorporated into micro/mesoporous supports or immobilized onto conductive electrodes and carbon materials
Several porous materials could be utilized to construct incorporated system containing a matrix that consisted of a diiron mimetic catalyst, a photosensitizer, and an electron donor, promoting photocatalytic HER in aqueous solution. Ott and co-workers had reported the incorporation of an organometallic diiron (dcbdt)[FeFe](CO)6 (dcbdt = 1,4-dicarboxylbenzene-2,3-ditiolate) (27, Scheme 3) into metal−organic framework (MOF) by postsynthetic exchange (PSE) of 1,4-benzenedicarboxylate (bdc) linker
Diiron dithiolates on the basis of peptides or proteins
Inspired by nature, the sophisticated organization of the outer coordination sphere of artificial H-cluster mimetics such as embedding the biomimetic active site within a peptide or protein scaffold had been prognosticated to provide a myriad of benefits beyond water compatibility, mechanism understanding, reactivity tuning of catalysis [110]. Initial work to tailor a diiron mimetic to a peptide framework was reported by Jones et al. in 2007 [111]. The diiron entity was anchored to the surface
Physical encapsulation
Cyclodextrins (CDs) consisted of hydrophobic cavities with a height of ca. 7.9 Å and discrepant diameters depending on the number of glucose units (Scheme 5) [122]. The unique cyclic oligosaccharides could serve as hosts for organometallics [123,124], while their hydrophilic hydroxyl rims provided hydrogen bonding sites [125]. The inclusion of a small molecule such as a diiron mimetic compound into the hydrophobic cavity of CD generated host–guest supramolecular system suitable for convenient
Metallopolymers [161,162]
To construct the photocatalytic HER system in aqueous solution, Wu and co-workers developed a diiron mimetic with hydrophilic oligomeric polyethylene glycol (PEG) chains covalently anchored to one iron atom through an iso-cyanide group (e.g. 73, Scheme 9) [163]. In combination with the MPA stabilized CdTe QDs as photosensitizer, H2A as proton source and SED, 73 mediated the hydrogen production in pure water with TON of up to 505 over 10 hours. The evaluation of the free-energy change and [FeIFe0
Conclusions and closing comments
Over the past two decades, significant advances have been achieved in engineering of synthetic water-soluble systems inspired by [FeFe]-hydrogenases for both electro- and photocatalytic HERs. However, the artificial catalytic systems that can achieve higher hydrogen productivities than natural hydrogenase are quite limited. The efficient and durable bioinspired HER in neutral or near-neutral aqueous solution is still under challenge in many aspects. For example, the active site in native
Acknowledgements
We are grateful to the National Natural Science Foundation of China (no. 21201022, 61106050, 61774023), the Specialized Research Fund for the Doctoral Program of Higher Education (no. 20122216120001), the Scientific and Technological "13th Five-Year Plan" Project of Jilin Provincial Department of Education (no. JJKH20170609KJ), the Scientific and Technological Development Project of Jilin Province (no. 20190101008JH) for financial support.
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