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Accounts of Chemical Research Nov 2015The development of technology for the inexpensive generation of the renewable energy vector H2 through water splitting is of immediate economic, ecological, and...
The development of technology for the inexpensive generation of the renewable energy vector H2 through water splitting is of immediate economic, ecological, and humanitarian interest. Recent interest in hydrogenases has been fueled by their exceptionally high catalytic rates for H2 production at a marginal overpotential, which is presently only matched by the nonscalable noble metal platinum. The mechanistic understanding of hydrogenase function guides the design of synthetic catalysts, and selection of a suitable hydrogenase enables direct applications in electro- and photocatalysis. [FeFe]-hydrogenases display excellent H2 evolution activity, but they are irreversibly damaged upon exposure to O2, which currently prevents their use in full water splitting systems. O2-tolerant [NiFe]-hydrogenases are known, but they are typically strongly biased toward H2 oxidation, while H2 production by [NiFe]-hydrogenases is often product (H2) inhibited. [NiFeSe]-hydrogenases are a subclass of [NiFe]-hydrogenases with a selenocysteine residue coordinated to the active site nickel center in place of a cysteine. They exhibit a combination of unique properties that are highly advantageous for applications in water splitting compared with other hydrogenases. They display a high H2 evolution rate with marginal inhibition by H2 and tolerance to O2. [NiFeSe]-hydrogenases are therefore one of the most active molecular H2 evolution catalysts applicable in water splitting. Herein, we summarize our recent progress in exploring the unique chemistry of [NiFeSe]-hydrogenases through biomimetic model chemistry and the chemistry with [NiFeSe]-hydrogenases in semiartificial photosynthetic systems. We gain perspective from the structural, spectroscopic, and electrochemical properties of the [NiFeSe]-hydrogenases and compare them with the chemistry of synthetic models of this hydrogenase active site. Our synthetic models give insight into the effects on the electronic properties and reactivity of the active site upon the introduction of selenium. We have utilized the exceptional properties of the [NiFeSe]-hydrogenase from Desulfomicrobium baculatum in a number of photocatalytic H2 production schemes, which are benchmark systems in terms of single site activity, tolerance toward O2, and in vitro water splitting with biological molecules. Each system comprises a light-harvesting component, which allows for light-driven electron transfer to the hydrogenase in order for it to catalyze H2 production. A system with [NiFeSe]-hydrogenase on a dye-sensitized TiO2 nanoparticle gives an enzyme-semiconductor hybrid for visible light-driven generation of H2 with an enzyme-based turnover frequency of 50 s(-1). A stable and inexpensive polymeric carbon nitride as a photosensitizer in combination with the [NiFeSe]-hydrogenase shows good activity for more than 2 days. Light-driven H2 evolution with the enzyme and an organic dye under high O2 levels demonstrates the excellent robustness and feasibility of water splitting with a hydrogenase-based scheme. This has led, most recently, to the development of a light-driven full water splitting system with a [NiFeSe]-hydrogenase wired to the water oxidation enzyme photosystem II in a photoelectrochemical cell. In contrast to the other systems, this photoelectrochemical system does not rely on a sacrificial electron donor and allowed us to establish the long sought after light-driven water splitting with an isolated hydrogenase.
Topics: Biomimetic Materials; Deltaproteobacteria; Desulfovibrio vulgaris; Hydrogenase; Photosynthesis; Selenocysteine
PubMed: 26488197
DOI: 10.1021/acs.accounts.5b00326 -
Biochimica Et Biophysica Acta Jun 2015The [FeFe]- and [NiFe]-hydrogenases catalyze the formal interconversion between hydrogen and protons and electrons, possess characteristic non-protein ligands at their... (Review)
Review
The [FeFe]- and [NiFe]-hydrogenases catalyze the formal interconversion between hydrogen and protons and electrons, possess characteristic non-protein ligands at their catalytic sites and thus share common mechanistic features. Despite the similarities between these two types of hydrogenases, they clearly have distinct evolutionary origins and likely emerged from different selective pressures. [FeFe]-hydrogenases are widely distributed in fermentative anaerobic microorganisms and likely evolved under selective pressure to couple hydrogen production to the recycling of electron carriers that accumulate during anaerobic metabolism. In contrast, many [NiFe]-hydrogenases catalyze hydrogen oxidation as part of energy metabolism and were likely key enzymes in early life and arguably represent the predecessors of modern respiratory metabolism. Although the reversible combination of protons and electrons to generate hydrogen gas is the simplest of chemical reactions, the [FeFe]- and [NiFe]-hydrogenases have distinct mechanisms and differ in the fundamental chemistry associated with proton transfer and control of electron flow that also help to define catalytic bias. A unifying feature of these enzymes is that hydrogen activation itself has been restricted to one solution involving diatomic ligands (carbon monoxide and cyanide) bound to an Fe ion. On the other hand, and quite remarkably, the biosynthetic mechanisms to produce these ligands are exclusive to each type of enzyme. Furthermore, these mechanisms represent two independent solutions to the formation of complex bioinorganic active sites for catalyzing the simplest of chemical reactions, reversible hydrogen oxidation. As such, the [FeFe]- and [NiFe]-hydrogenases are arguably the most profound case of convergent evolution. This article is part of a Special Issue entitled: Fe/S proteins: Analysis, structure, function, biogenesis and diseases.
Topics: Archaea; Archaeal Proteins; Bacteria; Bacterial Proteins; Genetic Variation; Hydrogen; Hydrogenase; Iron-Sulfur Proteins; Oxidation-Reduction; Phylogeny
PubMed: 25461840
DOI: 10.1016/j.bbamcr.2014.11.021 -
Trends in Biotechnology Nov 2022The vision to replace coal with hydrogen goes back to Jules Verne in 1874. However, sustainable hydrogen production remains challenging. The most elegant approach is to... (Review)
Review
The vision to replace coal with hydrogen goes back to Jules Verne in 1874. However, sustainable hydrogen production remains challenging. The most elegant approach is to utilize photosynthesis for water splitting and to subsequently save solar energy as hydrogen. Cyanobacteria and green algae are unicellular photosynthetic organisms that contain hydrogenases and thereby possess the enzymatic equipment for photosynthetic hydrogen production. These features of cyanobacteria and algae have inspired artificial and semi-artificial in vitro techniques, that connect photoexcited materials or enzymes with hydrogenases or mimics of these for hydrogen production. These in vitro methods have on their part been models for the fusion of cyanobacterial and algal hydrogenases to photosynthetic photosystem I (PSI) in vivo, which recently succeeded as proofs of principle.
Topics: Coal; Cyanobacteria; Hydrogen; Hydrogenase; Photosynthesis; Photosystem I Protein Complex; Water
PubMed: 35581021
DOI: 10.1016/j.tibtech.2022.04.007 -
International Journal of Molecular... Aug 2020Hydrogenases are complex metalloenzymes, showing tremendous potential as H-converting redox catalysts for application in light-driven H production, enzymatic fuel cells... (Review)
Review
Hydrogenases are complex metalloenzymes, showing tremendous potential as H-converting redox catalysts for application in light-driven H production, enzymatic fuel cells and H-driven cofactor regeneration. They catalyze the reversible oxidation of hydrogen into protons and electrons. The apo-enzymes are not active unless they are modified by a complicated post-translational maturation process that is responsible for the assembly and incorporation of the complex metal center. The catalytic center is usually easily inactivated by oxidation, and the separation and purification of the active protein is challenging. The understanding of the catalytic mechanisms progresses slowly, since the purification of the enzymes from their native hosts is often difficult, and in some case impossible. Over the past decades, only a limited number of studies report the homologous or heterologous production of high yields of hydrogenase. In this review, we emphasize recent discoveries that have greatly improved our understanding of microbial hydrogenases. We compare various heterologous hydrogenase production systems as well as in vitro hydrogenase maturation systems and discuss their perspectives for enhanced biohydrogen production. Additionally, activities of hydrogenases isolated from either recombinant organisms or in vivo/in vitro maturation approaches were systematically compared, and future perspectives for this research area are discussed.
Topics: Bacterial Proteins; Hydrogenase; Industrial Microbiology; Iron-Sulfur Proteins; Protein Engineering
PubMed: 32824336
DOI: 10.3390/ijms21165890 -
PloS One 2011[FeFe] hydrogenases are promising catalysts for producing hydrogen as a sustainable fuel and chemical feedstock, and they also serve as paradigms for biomimetic...
[FeFe] hydrogenases are promising catalysts for producing hydrogen as a sustainable fuel and chemical feedstock, and they also serve as paradigms for biomimetic hydrogen-evolving compounds. Hydrogen formation is catalyzed by the H-cluster, a unique iron-based cofactor requiring three carbon monoxide (CO) and two cyanide (CN⁻) ligands as well as a dithiolate bridge. Three accessory proteins (HydE, HydF, and HydG) are presumably responsible for assembling and installing the H-cluster, yet their precise roles and the biosynthetic pathway have yet to be fully defined. In this report, we describe effective cell-free methods for investigating H-cluster synthesis and [FeFe] hydrogenase activation. Combining isotopic labeling with FTIR spectroscopy, we conclusively show that each of the CO and CN⁻ ligands derive respectively from the carboxylate and amino substituents of tyrosine. Such in vitro systems with reconstituted pathways comprise a versatile approach for studying biosynthetic mechanisms, and this work marks a significant step towards an understanding of both the protein-protein interactions and complex reactions required for H-cluster assembly and hydrogenase maturation.
Topics: Bacterial Proteins; Carbon Monoxide; Cyanides; Hydrogen; Hydrogenase; Iron-Sulfur Proteins; Ligands; Models, Molecular; Molecular Structure; Protein Conformation; Spectroscopy, Fourier Transform Infrared; Tyrosine
PubMed: 21673792
DOI: 10.1371/journal.pone.0020346 -
Cyanobacterial hydrogenases and hydrogen metabolism revisited: recent progress and future prospects.International Journal of Molecular... May 2015Cyanobacteria have garnered interest as potential cell factories for hydrogen production. In conjunction with photosynthesis, these organisms can utilize inexpensive... (Review)
Review
Cyanobacteria have garnered interest as potential cell factories for hydrogen production. In conjunction with photosynthesis, these organisms can utilize inexpensive inorganic substrates and solar energy for simultaneous biosynthesis and hydrogen evolution. However, the hydrogen yield associated with these organisms remains far too low to compete with the existing chemical processes. Our limited understanding of the cellular hydrogen production pathway is a primary setback in the potential scale-up of this process. In this regard, the present review discusses the recent insight around ferredoxin/flavodoxin as the likely electron donor to the bidirectional Hox hydrogenase instead of the generally accepted NAD(P)H. This may have far reaching implications in powering solar driven hydrogen production. However, it is evident that a successful hydrogen-producing candidate would likely integrate enzymatic traits from different species. Engineering the [NiFe] hydrogenases for optimal catalytic efficiency or expression of a high turnover [FeFe] hydrogenase in these photo-autotrophs may facilitate the development of strains to reach target levels of biohydrogen production in cyanobacteria. The fundamental advancements achieved in these fields are also summarized in this review.
Topics: Cyanobacteria; Ferredoxins; Hydrogen; Hydrogenase; Iron-Sulfur Proteins; NADP
PubMed: 26006225
DOI: 10.3390/ijms160510537 -
Microbial Biotechnology Jul 2022Hydrogen is a clean alternative to fossil fuels. It has applications for electricity generation and transportation and is used for the manufacturing of ammonia and... (Review)
Review
Hydrogen is a clean alternative to fossil fuels. It has applications for electricity generation and transportation and is used for the manufacturing of ammonia and steel. However, today, H is almost exclusively produced from coal and natural gas. As such, methods to produce H that do not use fossil fuels need to be developed and adopted. The biological manufacturing of H may be one promising solution as this process is clean and renewable. Hydrogen is produced biologically via enzymes called hydrogenases. There are three classes of hydrogenases namely [FeFe], [NiFe] and [Fe] hydrogenases. The [FeFe] hydrogenase HydA1 from the model unicellular algae Chlamydomonas reinhardtii has been studied extensively and belongs to the A1 subclass of [FeFe] hydrogenases that have the highest turnover frequencies amongst hydrogenases (21,000 ± 12,000 H s for CaHydA from Clostridium acetobutyliticum). Yet to date, limitations in C. reinhardtii H production pathways have hampered commercial scale implementation, in part due to O sensitivity of hydrogenases and competing metabolic pathways, resulting in low H production efficiency. Here, we describe key processes in the biogenesis of HydA1 and H production pathways in C. reinhardtii. We also summarize recent advancements of algal H production using synthetic biology and describe valuable tools such as high-throughput screening (HTS) assays to accelerate the process of engineering algae for commercial biological H production.
Topics: Chlamydomonas reinhardtii; Fossil Fuels; Hydrogen; Hydrogenase; Synthetic Biology
PubMed: 35338590
DOI: 10.1111/1751-7915.14024 -
Structure (London, England : 1993) Aug 2011Hydrogenases are metalloenzymes that are key to energy metabolism in a variety of microbial communities. Divided into three classes based on their metal content, the... (Review)
Review
Hydrogenases are metalloenzymes that are key to energy metabolism in a variety of microbial communities. Divided into three classes based on their metal content, the [Fe]-, [FeFe]-, and [NiFe]-hydrogenases are evolutionarily unrelated but share similar nonprotein ligand assemblies at their active site metal centers that are not observed elsewhere in biology. These nonprotein ligands are critical in tuning enzyme reactivity, and their synthesis and incorporation into the active site clusters require a number of specific maturation enzymes. The wealth of structural information on different classes and different states of hydrogenase enzymes, biosynthetic intermediates, and maturation enzymes has contributed significantly to understanding the biochemistry of hydrogen metabolism. This review highlights the unique structural features of hydrogenases and emphasizes the recent biochemical and structural work that has created a clearer picture of the [FeFe]-hydrogenase maturation pathway.
Topics: Amino Acid Sequence; Bacterial Proteins; Catalytic Domain; Hydrogenase; Models, Molecular; Nonheme Iron Proteins; Oxidation-Reduction; Protein Processing, Post-Translational; Protein Structure, Secondary
PubMed: 21827941
DOI: 10.1016/j.str.2011.06.008 -
International Journal of Molecular... May 2023The extraordinary potential of hydrogen as a clean and sustainable fuel has sparked the interest of the scientific community to find environmentally friendly methods for... (Review)
Review
The extraordinary potential of hydrogen as a clean and sustainable fuel has sparked the interest of the scientific community to find environmentally friendly methods for its production. Biological catalysts are the most attractive solution, as they usually operate under mild conditions and do not produce carbon-containing byproducts. Hydrogenases promote reversible proton reduction to hydrogen in a variety of anoxic bacteria and algae, displaying unparallel catalytic performances. Attempts to use these sophisticated enzymes in scalable hydrogen production have been hampered by limitations associated with their production and stability. Inspired by nature, significant efforts have been made in the development of artificial systems able to promote the hydrogen evolution reaction, via either electrochemical or light-driven catalysis. Starting from small-molecule coordination compounds, peptide- and protein-based architectures have been constructed around the catalytic center with the aim of reproducing hydrogenase function into robust, efficient, and cost-effective catalysts. In this review, we first provide an overview of the structural and functional properties of hydrogenases, along with their integration in devices for hydrogen and energy production. Then, we describe the most recent advances in the development of homogeneous hydrogen evolution catalysts envisioned to mimic hydrogenases.
Topics: Protons; Hydrogen; Oxidation-Reduction; Hydrogenase; Photosynthesis; Catalysis
PubMed: 37239950
DOI: 10.3390/ijms24108605 -
Archaea (Vancouver, B.C.) 2015Hydrogen gas is a potential renewable alternative energy carrier that could be used in the future to help supplement humanity's growing energy needs. Unfortunately,... (Review)
Review
Hydrogen gas is a potential renewable alternative energy carrier that could be used in the future to help supplement humanity's growing energy needs. Unfortunately, current industrial methods for hydrogen production are expensive or environmentally unfriendly. In recent years research has focused on biological mechanisms for hydrogen production and specifically on hydrogenases, the enzyme responsible for catalyzing the reduction of protons to generate hydrogen. In particular, a better understanding of this enzyme might allow us to generate hydrogen that does not use expensive metals, such as platinum, as catalysts. The soluble hydrogenase I (SHI) from the hyperthermophile Pyrococcus furiosus, a member of the euryarchaeota, has been studied extensively and used in various biotechnological applications. This review summarizes the strategies used in engineering and characterizing three different forms of SHI and the properties of the recombinant enzymes. SHI has also been used in in vitro systems for hydrogen production and NADPH generation and these systems are also discussed.
Topics: Hydrogen; Hydrogenase; NADP; Pyrococcus furiosus; Recombinant Proteins
PubMed: 26543406
DOI: 10.1155/2015/912582