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Hydrogenase

From Wikipedia, the free encyclopedia

A hydrogenase is an enzyme that catalyses the reversible oxidation of molecular hydrogen (H2), as shown below:

H2 + Aox → 2H+ + Ared (1)
2H+ + Dred → H2 + Dox (2)

Hydrogen uptake (1) is coupled to the reduction of electron acceptors such as oxygen, nitrate, sulfate, carbon dioxide (CO2), and fumarate. On the other hand, proton reduction (2) is coupled to the oxidation of electron donors such as ferredoxin (FNR), and serves to dispose excess electrons in cells (essential in pyruvate fermentation). Both low-molecular weight compounds and proteins such as FNRs, cytochrome c3, and cytochrome c6 can act as physiological electron donors or acceptors for hydrogenases.[1]

Structural classification

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It has been estimated that 99% of all organisms utilize hydrogen, H2. Most of these species are microbes and their ability to use H2 as a metabolite arises from the expression of metalloenzymes known as hydrogenases.[2] Hydrogenases are sub-classified into three different types based on the active site metal content: iron-iron hydrogenase, nickel-iron hydrogenase, and iron hydrogenase.

The structures of the active sites of the three types of hydrogenase enzymes.

Hydrogenases catalyze, sometimes reversibly, H2 uptake. The [FeFe] and [NiFe] hydrogenases are true redox catalysts, driving H2 oxidation and proton (H+) reduction (equation 3), the [Fe] hydrogenases catalyze the reversible heterolytic cleavage of H2 shown by reaction (4).

H2 ⇌ 2 H+ + 2 e (3)
H2 ⇌ H+ + H (4)

Although originally believed to be "metal-free", the [Fe]-only hydrogenases contain Fe at the active site and no iron-sulfur clusters. [NiFe] and [FeFe] hydrogenases have some common features in their structures: Each enzyme has an active site and a few Fe-S clusters that are buried in protein. The active site, which is believed to be the place where catalysis takes place, is also a metallocluster, and each iron is coordinated by carbon monoxide (CO) and cyanide (CN) ligands.[3]

[NiFe] hydrogenase

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Crystal structure of [NiFe] hydrogenase

The [NiFe] hydrogenases are heterodimeric proteins consisting of small (S) and large (L) subunits. The small subunit contains three iron-sulfur clusters while the large subunit contains the active site, a nickel-iron centre which is connected to the solvent by a molecular tunnel.[4][5] In some [NiFe] hydrogenases, one of the Ni-bound cysteine residues is replaced by selenocysteine. On the basis of sequence similarity, however, the [NiFe] and [NiFeSe] hydrogenases should be considered a single superfamily. To date, periplasmic, cytoplasmic, and cytoplasmic membrane-bound hydrogenases have been found. The [NiFe] hydrogenases, when isolated, are found to catalyse both H2 evolution and uptake, with low-potential multihaem cytochromes such as cytochrome c3 acting as either electron donors or acceptors, depending on their oxidation state.[4] Generally speaking, however, [NiFe] hydrogenases are more active in oxidizing H2. A wide spectrum of H2 affinities have also been observed in H2-oxidizing hydrogenases.[6]

Like [FeFe] hydrogenases, [NiFe] hydrogenases are known to be usually deactivated by molecular oxygen (O2). Hydrogenase from Ralstonia eutropha, and several other so-called Knallgas-bacteria, were found to be oxygen-tolerant.[4][7] The soluble [NiFe] hydrogenase from Ralstonia eutropha H16 can be conveniently produced on heterotrophic growth media.[8][9] This finding increased hope that hydrogenases can be used in photosynthetic production of molecular hydrogen via splitting water. Another [NiFe], called Huc or Hyd1 or cyanobacterial-type uptake hydrogenase,[10] has been found to be oxygen insensitive while having a very high affinity for hydrogen. Hydrogen is able to penetrate narrow channels in the enzyme that oxygen molecules cannot enter. This allows bacteria such as Mycobacterium smegmatis to utilize the small amount of hydrogen in the atmosphere as a source of energy when other sources are lacking.[11][12]

[FeFe] hydrogenase

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Crystal structure of [FeFe] hydrogenase

The hydrogenases containing a di-iron center with a bridging dithiolate cofactor are called [FeFe] hydrogenases.[13] Three families of [FeFe] hydrogenases are recognized:

  • cytoplasmic, soluble, monomeric hydrogenases, found in strict anaerobes such as Clostridium pasteurianum and Megasphaera elsdenii. They catalyse both H2 evolution and uptake.
  • periplasmic, heterodimeric hydrogenases from Desulfovibrio spp., which can be purified aerobically.
  • soluble, monomeric hydrogenases, found in chloroplasts of green alga Scenedesmus obliquus, catalyses H2 evolution. The [Fe2S2] ferredoxin functions as natural electron donor linking the enzyme to the photosynthetic electron transport chain.

In contrast to [NiFe] hydrogenases, [FeFe] hydrogenases are generally more active in production of molecular hydrogen. Turnover frequency (TOF) in the order of 10,000 s−1 have been reported in literature for [FeFe] hydrogenases from Clostridium pasteurianum.[14] This has led to intense research focusing on use of [FeFe] hydrogenase for sustainable production of H2.[15]

The active site of the diiron hydrogenase is known as the H-cluster. The H-cluster consists of a [4Fe4S] cubane-shaped structure, coupled to the low valent diiron co-factor by a cysteine derived thiol. The diiron co-factor includes two iron atoms, connected by a bridging aza-dithiolate ligand (-SCH2-NH-CH2S-, adt), the iron atoms are coordinated by carbonyl and cyanide ligands.[16]

[FeFe]-hydrogenases can be separated into four distinct phylogenetic groups A−D.[17] Group A consists of prototypical and bifurcating [FeFe]-hydrogenases. In nature, prototypical [FeFe]-hydrogenases perform hydrogen turnover using ferredoxin as a redox partner while bifurcating types perform the same reaction using both ferredoxin and NAD(H) as electron donor or acceptor.[18] In order to conserve energy, anaerobic bacteria use electron bifurcation where exergonic and endergonic redox reactions are coupled to circumvent thermodynamic barriers. Group A comprises the best characterized and catalytically most active enzymes such as the [FeFe]-hydrogenase from Chlamydomonas reinhardtii (CrHydA1),[19] Desulfovibrio desulfuricans (DdHydAB or DdH),[20] and Clostridium pasteurianum and Clostridium acetobutylicum (CpHydA1 and CaHydA1, referred to as CpI and CaI).[21] No representative examples of Group B has been characterized yet but it is phylogenetically distinct even when it shares similar amino acid motifs around the H-cluster as Group A [FeFe]-hydrogenases. Group C has been classified as "sensory" based on the presence of a Per-Arnt-Sim domain.[22][23] One example of a Group C [FeFe]-hydrogenase is from Thermotoga maritima (TmHydS) which shows only modest catalytic rates compared to Group A enzymes and an apparent high sensitivity toward hydrogen (H2).[24] A closely related subclass from Group D has a similar location on the bacterial gene and share similar domain structure to a subclass from Group E but it lacks the PAS domain.[17][22] Within Group D, the [FeFe]-hydrogenase from Thermoanaerobacter mathranii (referred to as Tam HydS) has been characterized.[25]

[Fe]-only hydrogenase

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Crystal structure of [Fe] hydrogenase

5,10-methenyltetrahydromethanopterin hydrogenase (EC 1.12.98.2) found in methanogenic Archaea contains neither nickel nor iron-sulfur clusters but an iron-containing cofactor that was recently characterized by X-ray diffraction.[26]

Unlike the other two types, [Fe]-only hydrogenases are found only in some hydrogenotrophic methanogenic archaea. They also feature a fundamentally different enzymatic mechanism in terms of redox partners and how electrons are delivered to the active site. In [NiFe] and [FeFe] hydrogenases, electrons travel through a series of metallorganic clusters that comprise a long distance; the active site structures remain unchanged during the whole process. In [Fe]-only hydrogenases, however, electrons are directly delivered to the active site via a short distance. Methenyl-H4MPT+, a cofactor, directly accepts the hydride from H2 in the process. [Fe]-only hydrogenase is also known as H2-forming methylenetetrahydromethanopterin (methylene-H4MPT) dehydrogenase, because its function is the reversible reduction of methenyl-H4MPT+ to methylene-H4MPT.[27] The hydrogenation of a methenyl-H4MPT+ occurs instead of H2 oxidation/production, which is the case for the other two types of hydrogenases. While the exact mechanism of the catalysis is still under study, recent finding suggests that molecular hydrogen is first heterolytically cleaved by Fe(II), followed by transfer of hydride to the carbocation of the acceptor.[28]

Mechanism

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The molecular mechanism by which protons are converted into hydrogen molecules within hydrogenases is still under extensive study. One popular approach employs mutagenesis to elucidate roles of amino acids and/or ligands in different steps of catalysis such as intramolecular transport of substrates. For instance, Cornish et al. conducted mutagenesis studies and found out that four amino acids located along the putative channel connecting the active site and protein surface are critical to enzymatic function of [FeFe] hydrogenase from Clostridium pasteurianum (CpI).[29] On the other hand, one can also rely on computational analysis and simulations. Nilsson Lill and Siegbahn have recently taken this approach in investigating the mechanism by which [NiFe] hydrogenases catalyze H2 cleavage.[30] The two approaches are complementary and can benefit one another. In fact, Cao and Hall combined both approaches in developing the model that describes how hydrogen molecules are oxidized or produced within the active site of [FeFe] hydrogenases.[31] While more research and experimental data are required to complete our understanding of the mechanism, these findings have allowed scientists to apply the knowledge in, e.g., building artificial catalysts mimicking active sites of hydrogenases.[32]

Biological function

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Assuming that the Earth's atmosphere was initially rich in hydrogen, scientists hypothesize that hydrogenases were evolved to generate energy from/as molecular H2. Accordingly, hydrogenases can either help microorganisms to proliferate under such conditions, or to set up ecosystems empowered by H2.[33] Microbial communities driven by molecular hydrogen have, in fact, been found in deep-sea settings where other sources of energy from photosynthesis are not available. Based on these grounds, the primary role of hydrogenases are believed to be energy generation, and this can be sufficient to sustain an ecosystem.

Recent studies have revealed other biological functions of hydrogenases. To begin with, bidirectional hydrogenases can also act as "valves" to control excess reducing equivalents, especially in photosynthetic microorganisms. Such a role makes hydrogenases play a vital role in anaerobic metabolism.[34][35] Moreover, hydrogenases may also be involved in membrane-linked energy conservation through the generation of a transmembrane protonmotive force.[15]There is a possibility that hydrogenases have been responsible for bioremediation of chlorinated compounds. Hydrogenases proficient in H2 uptake can help heavy metal contaminants to be recovered in intoxicated forms. These uptake hydrogenases have been recently discovered in pathogenic bacteria and parasites and are believed to be involved in their virulence.[15]

Applications

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Hydrogenases were first discovered in the 1930s,[36] and they have since attracted interest from many researchers including inorganic chemists who have synthesized a variety of hydrogenase mimics. The soluble [NiFe] hydrogenase from Ralstonia eutropha H16 is a promising candidate enzyme for H2-based biofuel application as it favours H2 oxidation and is relatively oxygen-tolerant. It can be produced on heterotrophic growth media[8] and purified via anion exchange and size exclusion chromatography matrices.[9] Understanding the catalytic mechanism of hydrogenase might help scientists design clean biological energy sources, such as algae, that produce hydrogen.[37]

Biological hydrogen production

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Various systems are capable of splitting water into O2 and H+ from incident sunlight. Likewise, numerous catalysts, either chemical or biological, can reduce the produced H+ into H2. Different catalysts require unequal overpotential for this reduction reaction to take place. Hydrogenases are attractive since they require a relatively low overpotential. In fact, its catalytic activity is more effective than platinum, which is the best known catalyst for H2 evolution reaction.[38] Among three different types of hydrogenases, [FeFe] hydrogenases is considered as a strong candidate for an integral part of the solar H2 production system since they offer an additional advantage of high TOF (over 9000 s−1)[6].

Low overpotential and high catalytic activity of [FeFe] hydrogenases are accompanied by high O2 sensitivity. It is necessary to engineer them O2-tolerant for use in solar H2 production since O2 is a by-product of water splitting reaction. Past research efforts by various groups around the world have focused on understanding the mechanisms involved in O2-inactivation of hydrogenases.[5][39] For instance, Stripp et al. relied on protein film electrochemistry and discovered that O2 first converts into a reactive species at the active site of [FeFe] hydrogenases, and then damages its [4Fe-4S] domain.[40] Cohen et al. investigated how oxygen can reach the active site that is buried inside the protein body by molecular dynamics simulation approach; their results indicate that O2 diffuses through mainly two pathways that are formed by enlargement of and interconnection between cavities during dynamic motion.[41] These works, in combination with other reports, suggest that inactivation is governed by two phenomena: diffusion of O2 to the active site, and destructive modification of the active site.

Despite these findings, research is still under progress for engineering oxygen tolerance in hydrogenases. While researchers have found oxygen-tolerant [NiFe] hydrogenases, they are only efficient in hydrogen uptake and not production[21]. Bingham et al.'s recent success in engineering [FeFe] hydrogenase from Clostridium pasteurianum was also limited to retained activity (during exposure to oxygen) for H2 consumption, only.[42]

Hydrogenase-based biofuel cells

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Typical enzymatic biofuel cells involve the usage of enzymes as electrocatalysts at either both cathode and anode or at one electrode. In hydrogenase-based biofuel cells, hydrogenase enzymes are present at the anode for H2 oxidation.[9][4][43]

Principle

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The bidirectional or reversible reaction catalyzed by hydrogenase allows for the capture and storage of renewable energy as fuel with use on demand. This can be demonstrated through the chemical storage of electricity obtained from a renewable source (e.g. solar, wind, hydrothermal) as H2 during periods of low energy demands. When energy is desired, H2 can be oxidized to produce electricity.[43]

Advantages

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This is one solution to the challenge in the development of technologies for the capture and storage of renewable energy as fuel with use on demand. The generation of electricity from H2 is comparable with the similar functionality of Platinum catalysts minus the catalyst poisoning, and thus is very efficient. In the case of H2/O2 fuel cells, where the product is water, there is no production of greenhouse gases.[43]

Biochemical classification

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EC 1.12.1.2

hydrogen dehydrogenase (hydrogen:NAD+ oxidoreductase)

H2 + NAD+ ⇌ H+ + NADH
EC 1.12.1.3

hydrogen dehydrogenase (NADP) (hydrogen:NADPH+ oxidoreductase)

H2 + NADP+ ⇌ H+ + NADPH
EC 1.12.2.1

cytochrome-c3 hydrogenase (hydrogen:ferricytochrome-c3 oxidoreductase)

2H2 + ferricytochrome c3 ⇌ 4H+ + ferrocytochrome c3
EC 1.12.5.1

hydrogen:quinone oxidoreductase

H2 + menaquinone ⇌ menaquinol
EC 1.12.7.2

ferredoxin hydrogenase (hydrogen:ferredoxin oxidoreductase)

H2 + oxidized ferredoxin ⇌ 2H+ + reduced ferredoxin
EC 1.12.98.1

coenzyme F420 hydrogenase (hydrogen:coenzyme F420 oxidoreductase)

H2 + coenzyme F420 ⇌ reduced coenzyme F420
EC 1.12.99.6

hydrogenase (acceptor) (hydrogen:acceptor oxidoreductase)

H2 + A ⇌ AH2
EC 1.12.98.2

5,10-methenyltetrahydromethanopterin hydrogenase (hydrogen:5,10-methenyltetrahydromethanopterin oxidoreductase)

H2 + 5,10-methenyltetrahydromethanopterin ⇌ H+ + 5,10-methylenetetrahydromethanopterin
EC 1.12.98.3

Methanosarcina-phenazine hydrogenase [hydrogen:2-(2,3-dihydropentaprenyloxy)phenazine oxidoreductase]

H2 + 2-(2,3-dihydropentaprenyloxy)phenazine ⇌ 2-dihydropentaprenyloxyphenazine

References

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  1. ^ Vignais PM, Billoud B, Meyer J (August 2001). "Classification and phylogeny of hydrogenases". FEMS Microbiology Reviews. 25 (4): 455–501. doi:10.1111/j.1574-6976.2001.tb00587.x. PMID 11524134.
  2. ^ Lubitz W, Ogata H, Rüdiger O, Reijerse E (April 2014). "Hydrogenases". Chemical Reviews. 114 (8): 4081–4148. doi:10.1021/cr4005814. PMID 24655035.
  3. ^ Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (October 2007). "Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases". Chemical Reviews. 107 (10): 4273–4303. doi:10.1021/cr050195z. PMID 17850165.
  4. ^ a b c d Jugder BE, Welch J, Aguey-Zinsou KF, Marquis CP (2013-05-14). "Fundamentals and electrochemical applications of [Ni–Fe]-uptake hydrogenases". RSC Advances. 3 (22): 8142. Bibcode:2013RSCAd...3.8142J. doi:10.1039/c3ra22668a. ISSN 2046-2069.
  5. ^ a b Liebgott PP, Leroux F, Burlat B, Dementin S, Baffert C, Lautier T, et al. (January 2010). "Relating diffusion along the substrate tunnel and oxygen sensitivity in hydrogenase". Nature Chemical Biology. 6 (1): 63–70. doi:10.1038/nchembio.276. PMID 19966788.
  6. ^ Greening C, Berney M, Hards K, Cook GM, Conrad R (March 2014). "A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases". Proceedings of the National Academy of Sciences of the United States of America. 111 (11): 4257–4261. Bibcode:2014PNAS..111.4257G. doi:10.1073/pnas.1320586111. PMC 3964045. PMID 24591586.
  7. ^ Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, et al. (2005). "[NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation". Journal of Molecular Microbiology and Biotechnology. 10 (2–4): 181–196. doi:10.1159/000091564. PMID 16645314. S2CID 8030367.
  8. ^ a b Jugder BE, Chen Z, Ping DT, Lebhar H, Welch J, Marquis CP (March 2015). "An analysis of the changes in soluble hydrogenase and global gene expression in Cupriavidus necator (Ralstonia eutropha) H16 grown in heterotrophic diauxic batch culture". Microbial Cell Factories. 14 (1): 42. doi:10.1186/s12934-015-0226-4. PMC 4377017. PMID 25880663.
  9. ^ a b c Jugder BE, Lebhar H, Aguey-Zinsou KF, Marquis CP (2016-01-01). "Production and purification of a soluble hydrogenase from Ralstonia eutropha H16 for potential hydrogen fuel cell applications". MethodsX. 3: 242–250. doi:10.1016/j.mex.2016.03.005. PMC 4816682. PMID 27077052.
  10. ^ Cordero PR, Grinter R, Hards K, Cryle MJ, Warr CG, Cook GM, et al. (December 2019). "Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence". The Journal of Biological Chemistry. 294 (50): 18980–18991. doi:10.1074/jbc.RA119.011076. PMC 6916507. PMID 31624148.
  11. ^ Grinter R, Kropp A, Venugopal H, Senger M, Badley J, Cabotaje PR, et al. (March 2023). "Structural basis for bacterial energy extraction from atmospheric hydrogen". Nature. 615 (7952): 541–547. Bibcode:2023Natur.615..541G. doi:10.1038/s41586-023-05781-7. PMC 10017518. PMID 36890228.
  12. ^ Wilkins A (Mar 8, 2023). "Soil bacteria enzyme generates electricity from hydrogen in the air". New Scientist. 257 (3430): 13. Bibcode:2023NewSc.257...13W. doi:10.1016/S0262-4079(23)00459-1. S2CID 257625443.
  13. ^ Berggren G, Adamska A, Lambertz C, Simmons TR, Esselborn J, Atta M, et al. (July 2013). "Biomimetic assembly and activation of [FeFe]-hydrogenases". Nature. 499 (7456): 66–69. Bibcode:2013Natur.499...66B. doi:10.1038/nature12239. PMC 3793303. PMID 23803769.
  14. ^ Madden C, Vaughn MD, Díez-Pérez I, Brown KA, King PW, Gust D, et al. (January 2012). "Catalytic turnover of [FeFe]-hydrogenase based on single-molecule imaging". Journal of the American Chemical Society. 134 (3): 1577–1582. doi:10.1021/ja207461t. PMID 21916466.
  15. ^ Smith PR, Bingham AS, Swartz JR (2012). "Generation of hydrogen from NADPH using an [FeFe] hydrogenase". International Journal of Hydrogen Energy. 37 (3): 2977–2983. doi:10.1016/j.ijhydene.2011.03.172.
  16. ^ Németh B, Esmieu C, Redman HJ, Berggren G (May 2019). "Monitoring H-cluster assembly using a semi-synthetic HydF protein". Dalton Transactions. 48 (18): 5978–5986. doi:10.1039/C8DT04294B. PMC 6509880. PMID 30632592.
  17. ^ a b Land H, Senger M, Berggren G, Stripp ST (2020-05-28). "Current State of [FeFe]-Hydrogenase Research: Biodiversity and Spectroscopic Investigations". ACS Catalysis. 10 (13): 7069–7086. doi:10.1021/acscatal.0c01614. ISSN 2155-5435. S2CID 219749715.
  18. ^ Schuchmann K, Chowdhury NP, Müller V (2018-12-04). "Complex Multimeric [FeFe] Hydrogenases: Biochemistry, Physiology and New Opportunities for the Hydrogen Economy". Frontiers in Microbiology. 9: 2911. doi:10.3389/fmicb.2018.02911. PMC 6288185. PMID 30564206.
  19. ^ Happe T, Naber JD (June 1993). "Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii". European Journal of Biochemistry. 214 (2): 475–481. doi:10.1111/j.1432-1033.1993.tb17944.x. PMID 8513797.
  20. ^ Glick BR, Martin WG, Martin SM (October 1980). "Purification and properties of the periplasmic hydrogenase from Desulfovibrio desulfuricans". Canadian Journal of Microbiology. 26 (10): 1214–1223. doi:10.1139/m80-203. PMID 7006765.
  21. ^ Nakos G, Mortenson L (March 1971). "Purification and properties of hydrogenase, an iron sulfur protein, from Clostridium pasteurianum W5". Biochimica et Biophysica Acta (BBA) - Enzymology. 227 (3): 576–583. doi:10.1016/0005-2744(71)90008-8. PMID 5569125.
  22. ^ a b Calusinska M, Happe T, Joris B, Wilmotte A (June 2010). "The surprising diversity of clostridial hydrogenases: a comparative genomic perspective". Microbiology. 156 (Pt 6): 1575–1588. doi:10.1099/mic.0.032771-0. PMID 20395274.
  23. ^ Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, et al. (March 2016). "Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival". The ISME Journal. 10 (3): 761–777. Bibcode:2016ISMEJ..10..761G. doi:10.1038/ismej.2015.153. PMC 4817680. PMID 26405831.
  24. ^ Chongdar N, Birrell JA, Pawlak K, Sommer C, Reijerse EJ, Rüdiger O, et al. (January 2018). "Unique Spectroscopic Properties of the H-Cluster in a Putative Sensory [FeFe] Hydrogenase". Journal of the American Chemical Society. 140 (3): 1057–1068. doi:10.1021/jacs.7b11287. PMID 29251926.
  25. ^ Land H, Sekretareva A, Huang P, Redman HJ, Németh B, Polidori N, et al. (September 2020). "Characterization of a putative sensory [FeFe]-hydrogenase provides new insight into the role of the active site architecture". Chemical Science. 11 (47): 12789–12801. doi:10.1039/D0SC03319G. PMC 8163306. PMID 34094474.
  26. ^ Shima S, Pilak O, Vogt S, Schick M, Stagni MS, Meyer-Klaucke W, et al. (July 2008). "The crystal structure of [Fe]-hydrogenase reveals the geometry of the active site". Science. 321 (5888): 572–575. Bibcode:2008Sci...321..572S. doi:10.1126/science.1158978. PMID 18653896. S2CID 206513302.
  27. ^ Salomone-Stagni M, Stellato F, Whaley CM, Vogt S, Morante S, Shima S, et al. (March 2010). "The iron-site structure of [Fe]-hydrogenase and model systems: an X-ray absorption near edge spectroscopy study". Dalton Transactions. 39 (12): 3057–3064. doi:10.1039/b922557a. PMC 3465567. PMID 20221540.
  28. ^ Shima S, Vogt S, Göbels A, Bill E (December 2010). "Iron-chromophore circular dichroism of [Fe]-hydrogenase: the conformational change required for H2 activation". Angewandte Chemie. 49 (51): 9917–9921. doi:10.1002/anie.201006255. PMID 21105038.
  29. ^ Cornish AJ, Gärtner K, Yang H, Peters JW, Hegg EL (November 2011). "Mechanism of proton transfer in [FeFe]-hydrogenase from Clostridium pasteurianum". The Journal of Biological Chemistry. 286 (44): 38341–38347. doi:10.1074/jbc.M111.254664. PMC 3207428. PMID 21900241.
  30. ^ Lill SO, Siegbahn PE (February 2009). "An autocatalytic mechanism for NiFe-hydrogenase: reduction to Ni(I) followed by oxidative addition". Biochemistry. 48 (5): 1056–1066. doi:10.1021/bi801218n. PMID 19138102.
  31. ^ Cao Z, Hall MB (April 2001). "Modeling the active sites in metalloenzymes. 3. Density functional calculations on models for [Fe]-hydrogenase: structures and vibrational frequencies of the observed redox forms and the reaction mechanism at the Diiron Active Center". Journal of the American Chemical Society. 123 (16): 3734–3742. doi:10.1021/ja000116v. PMID 11457105.
  32. ^ Tard C, Liu X, Ibrahim SK, Bruschi M, De Gioia L, Davies SC, et al. (February 2005). "Synthesis of the H-cluster framework of iron-only hydrogenase". Nature. 433 (7026): 610–613. Bibcode:2005Natur.433..610T. doi:10.1038/nature03298. PMID 15703741. S2CID 4430994.
  33. ^ Vignais PM, Billoud B (October 2007). "Occurrence, classification, and biological function of hydrogenases: an overview". Chemical Reviews. 107 (10): 4206–4272. doi:10.1021/cr050196r. PMID 17927159.
  34. ^ Adams MW, Stiefel EI (December 1998). "Biological hydrogen production: not so elementary". Science. 282 (5395): 1842–1843. doi:10.1126/science.282.5395.1842. PMID 9874636. S2CID 38018712.
  35. ^ Frey M (March 2002). "Hydrogenases: hydrogen-activating enzymes". ChemBioChem. 3 (2–3): 153–160. doi:10.1002/1439-7633(20020301)3:2/3<153::AID-CBIC153>3.0.CO;2-B. PMID 11921392. S2CID 36754174.
  36. ^ Thauer RK (September 1998). "Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture". Microbiology. 144 (Pt 9): 2377–2406. doi:10.1099/00221287-144-9-2377. PMID 9782487.
  37. ^ Florin L, Tsokoglou A, Happe T (March 2001). "A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain". The Journal of Biological Chemistry. 276 (9): 6125–6132. doi:10.1074/jbc.M008470200. PMID 11096090.
  38. ^ Hinnemann B, Moses PG, Bonde J, Jørgensen KP, Nielsen JH, Horch S, et al. (April 2005). "Biomimetic hydrogen evolution: MoS2 nanoparticles as catalyst for hydrogen evolution". Journal of the American Chemical Society. 127 (15): 5308–5309. doi:10.1021/ja0504690. PMID 15826154.
  39. ^ Goris T, Wait AF, Saggu M, Fritsch J, Heidary N, Stein M, et al. (May 2011). "A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase". Nature Chemical Biology. 7 (5): 310–318. doi:10.1038/nchembio.555. PMID 21390036.
  40. ^ Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, Haumann M, et al. (October 2009). "How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms". Proceedings of the National Academy of Sciences of the United States of America. 106 (41): 17331–17336. Bibcode:2009PNAS..10617331S. doi:10.1073/pnas.0905343106. PMC 2765078. PMID 19805068.
  41. ^ Cohen J, Kim K, King P, Seibert M, Schulten K (September 2005). "Finding gas diffusion pathways in proteins: application to O2 and H2 transport in CpI [FeFe]-hydrogenase and the role of packing defects". Structure. 13 (9): 1321–1329. doi:10.1016/j.str.2005.05.013. PMID 16154089.
  42. ^ Bingham AS, Smith PR, Swartz JR (2012). "Evolution of an [FeFe] hydrogenase with decreased oxygen sensitivity". International Journal of Hydrogen Energy. 37 (3): 2965–2976. doi:10.1016/j.ijhydene.2011.02.048.
  43. ^ a b c Lubitz W, Ogata H, Rüdiger O, Reijerse E (April 2014). "Hydrogenases". Chemical Reviews. 114 (8): 4081–4148. doi:10.1021/cr4005814. PMID 24655035.
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