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Nickel-centred proton reduction catalysis in a model of [NiFe] hydrogenase

Nature Chemistry volume 8, pages 1054–1060 (2016)Cite this article

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Abstract

Hydrogen production through water splitting is one of the most promising solutions for the storage of renewable energy. [NiFe] hydrogenases are organometallic enzymes containing nickel and iron centres that catalyse hydrogen evolution with performances that rival those of platinum. These enzymes provide inspiration for the design of new molecular catalysts that do not require precious metals. However, all heterodinuclear NiFe models reported so far do not reproduce the Ni-centred reactivity found at the active site of [NiFe] hydrogenases. Here, we report a structural and functional NiFe mimic that displays reactivity at the Ni site. This is shown by the detection of two catalytic intermediates that reproduce structural and electronic features of the Ni-L and Ni-R states of the enzyme during catalytic turnover. Under electrocatalytic conditions, this mimic displays high rates for H2 evolution (second-order rate constant of 2.5 × 104 M−1 s−1; turnover frequency of 250 s−1 at 10 mM H+ concentration) from mildly acidic solutions.

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Figure 1: Active site and H2 production catalytic cyclic of [NiFe] hydrogenase.
Figure 2: Synthesis and X-ray structure of LN2S2NiIIFeII.
Figure 3: DFT-optimized structures and principal spectroscopic characterizations of LN2S2NiIIFeII, LN2S2NiIFeII and LN2S2NiII(H)FeII.
Figure 4: Electrocatalytic properties for H2 production of LN2S2NiIIFeII.
Figure 5: H2 production catalytic cycle of LN2S2NiIIFeII.

References

  1. Volbeda, A. et al. Crystal structure of the nickel–iron hydrogenase from Desulfovibrio gigas. Nature 373, 580–587 (1995).

    Article  CAS  PubMed  Google Scholar 

  2. Lubitz, W., Ogata, H., Rüdiger, O. & Reijerse, E. Hydrogenases. Chem. Rev. 114, 4081–4148 (2014).

    Article  CAS  PubMed  Google Scholar 

  3. Foerster, S. et al. Single crystal EPR studies of the reduced active site of [NiFe] hydrogenase from Desulfovibrio vulgaris miyazaki F. J. Am. Chem. Soc. 125, 83–93 (2003).

    Article  CAS  PubMed  Google Scholar 

  4. Brecht, M., van Gastel, M., Buhrke, T., Friedrich, B. & Lubitz, W. Direct detection of a hydrogen ligand in the [NiFe] center of the regulatory H2-sensing hydrogenase from Ralstonia eutropha in its reduced state by HYSCORE and ENDOR spectroscopy. J. Am. Chem. Soc. 125, 13075–13083 (2003).

    Article  CAS  PubMed  Google Scholar 

  5. George, S. J., Kurkin, S., Thorneley, R. N. F. & Albracht, S. P. J. Reactions of H2, CO, and O2 with active [NiFe]-hydrogenase from Allochromatium vinosum. A stopped-flow infrared study. Biochemistry 43, 6808–6819 (2004).

    Article  CAS  PubMed  Google Scholar 

  6. Ogata, H., Nishikawa, K. & Lubitz, W. Hydrogens detected by subatomic resolution protein crystallography in a [NiFe] hydrogenase. Nature 520, 571–574 (2015).

    Article  CAS  PubMed  Google Scholar 

  7. van der Zwaan, J. W., Albracht, S. P. J., Fontijn, R. D. & Slater, E. C. Monovalent nickel in hydrogenase from Chromatium vinosum: light sensitivity and evidence for direct interaction with hydrogen. FEBS Lett. 179, 271–277 (1985).

    Article  CAS  PubMed  Google Scholar 

  8. Murphy, B. J. et al. Discovery of dark pH-dependent H+ migration in a [NiFe]-hydrogenase and its mechanistic relevance: mobilizing the hydrido ligand of the Ni–C intermediate. J. Am. Chem. Soc. 137, 8484–8489 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hidalgo, R., Ash, P. A., Healy, A. J. & Vincent, K. A. Infrared spectroscopy during electrocatalytic turnover reveals the Ni–L active site state during H2 oxidation by a NiFe hydrogenase. Angew. Chem. Int. Ed. 54, 7110–7113 (2015).

    Article  CAS  Google Scholar 

  10. Tard, C. & Pickett, C. J. Structural and functional analogues of the active sites of the [Fe]-, [NiFe]-, and [FeFe]-hydrogenases. Chem. Rev. 109, 2245–2274 (2009).

    Article  CAS  PubMed  Google Scholar 

  11. Ohki, Y. & Tatsumi, K. Thiolate-bridged iron–nickel models for the active site of [NiFe] hydrogenase. Eur. J. Inorg. Chem. 2011, 973–985 (2011).

    Article  CAS  Google Scholar 

  12. Simmons, T. R., Berggren, G., Bacchi, M., Fontecave, M. & Artero, V. Mimicking hydrogenases: from biomimetics to artificial enzymes. Coord. Chem. Rev. 270–271, 127–150 (2014).

    Article  CAS  Google Scholar 

  13. Kaur-Ghumaan, S. & Stein, M. [NiFe] hydrogenases: how close do structural and functional mimics approach the active site? Dalton Trans. 43, 9392–9405 (2014).

    Article  CAS  PubMed  Google Scholar 

  14. Fourmond, V. et al. A nickel–manganese catalyst as a biomimic of the active site of NiFe hydrogenases: a combined electrocatalytical and DFT mechanistic study. Energy Environ. Sci. 4, 2417–2427 (2011).

    Article  CAS  Google Scholar 

  15. Song, L.-C., Li, J.-P., Xie, Z.-J. & Song, H.-B. Synthesis, structural characterization, and electrochemical properties of dinuclear Ni/Mn model complexes for the active site of [NiFe]-hydrogenases. Inorg. Chem. 52, 11618–11626 (2013).

    Article  CAS  PubMed  Google Scholar 

  16. Ogo, S. et al. A dinuclear Ni(µ-H)Ru complex derived from H2 . Science 316, 585–587 (2007).

    Article  CAS  PubMed  Google Scholar 

  17. Canaguier, S., Fontecave, M. & Artero, V. Cp*-ruthenium-nickel-based H2-evolving electrocatalysts as bio-inspired models of NiFe hydrogenases. Eur. J. Inorg. Chem. 2011, 1094–1099 (2011).

    Article  CAS  Google Scholar 

  18. Canaguier, S. et al. Catalytic hydrogen production by a Ni–Ru mimic of NiFe hydrogenases involves a proton-coupled electron transfer step. Chem. Commun. 49, 5004–5006 (2013).

    Article  CAS  Google Scholar 

  19. Oudart, Y., Artero, V., Pécaut, J., Lebrun, C. & Fontecave, M. Dinuclear nickel–ruthenium complexes as functional bio-inspired models of NiFe hydrogenases. Eur. J. Inorg. Chem. 2007, 2613–2626 (2007).

    Article  CAS  Google Scholar 

  20. Denny, J. A. & Darensbourg, M. Y. Metallodithiolates as ligands in coordination, bioinorganic, and organometallic chemistry. Chem. Rev. 115, 5248–5273 (2015).

    Article  CAS  PubMed  Google Scholar 

  21. Ogo, S. et al. A functional [NiFe] hydrogenase mimic that catalyzes electron and hydride transfer from H2 . Science 339, 682–684 (2013).

    Article  CAS  PubMed  Google Scholar 

  22. Barton, B. E. & Rauchfuss, T. B. Hydride-containing models for the active site of the nickel–iron hydrogenases. J. Am. Chem. Soc. 132, 14877–14885 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Barton, B. E., Whaley, C. M., Rauchfuss, T. B. & Gray, D. L. Nickel–iron dithiolato hydrides relevant to the [NiFe]-hydrogenase active site. J. Am. Chem. Soc. 131, 6942–6943 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Vaccaro, L., Artero, V., Canaguier, S., Fontecave, M. & Field, M. J. Mechanism of hydrogen evolution catalyzed by NiFe hydrogenases: insights from a Ni–Ru model compound. Dalton Trans. 39, 3043–3049 (2010).

    Article  CAS  PubMed  Google Scholar 

  25. Simmons, T. R. & Artero, V. Catalytic hydrogen oxidation: dawn of a new iron age. Angew. Chem. Int. Ed. 52, 6143–6145 (2013).

    Article  CAS  Google Scholar 

  26. Chambers, G. M. et al. Models of the Ni–L and Ni–SIa states of the [NiFe]-hydrogenase active site. Inorg. Chem. 55, 419–431 (2016).

    Article  CAS  PubMed  Google Scholar 

  27. Gennari, M. et al. Influence of mixed thiolate/thioether versus dithiolate coordination on the accessibility of the uncommon +I and +III oxidation states for the nickel ion: an experimental and computational study. Inorg. Chem. 50, 3707–3716 (2011).

    Article  CAS  PubMed  Google Scholar 

  28. Gennari, M. et al. Reversible apical coordination of imidazole between the Ni(III) and Ni(II) oxidation states of a dithiolate complex: a process related to the Ni superoxide dismutase. Inorg. Chem. 49, 6399–6401 (2010).

    Article  CAS  PubMed  Google Scholar 

  29. Canaguier, S. et al. A structural and functional mimic of the active site of NiFe hydrogenases. Chem. Commun. 46, 5876–5878 (2010).

    Article  CAS  Google Scholar 

  30. Zhu, W. et al. Modulation of the electronic structure and the Ni–Fe distance in heterobimetallic models for the active site in [NiFe] hydrogenase. Proc. Natl Acad. Sci. USA 102, 18280–18285 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Darensbourg, D. J., Reibenspies, J. H., Lai, C.-H., Lee, W.-Z. & Darensbourg, M. Y. Analysis of an organometallic iron site model for the heterodimetallic unit of [NiFe] hydrogenase. J. Am. Chem. Soc. 119, 7903–7904 (1997).

    Article  CAS  Google Scholar 

  32. Pandelia, M.-E., Ogata, H. & Lubitz, W. Intermediates in the catalytic cycle of [NiFe] hydrogenase: functional spectroscopy of the active site. ChemPhysChem 11, 1127–1140 (2010).

    Article  CAS  PubMed  Google Scholar 

  33. Roncaroli, F. et al. Cofactor composition and function of a H2-sensing regulatory hydrogenase as revealed by Mossbauer and EPR spectroscopy. Chem. Sci. 6, 4495–4507 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lubitz, W., Gastel, M. V. & Gärtner, W. in Nickel and its Surprising Impact in Nature (eds Sigel, A., Sigel, H. & Sigel, R. K. O.) 279–322 (Wiley, 2007).

    Book  Google Scholar 

  35. Roy, S., Groy, T. L. & Jones, A. K. Biomimetic model for [FeFe]-hydrogenase: asymmetrically disubstituted diiron complex with a redox-active 2,2′-bipyridyl ligand. Dalton Trans. 42, 3843–3853 (2013).

    Article  CAS  PubMed  Google Scholar 

  36. Farmer, P. J., Reibenspies, J. H., Lindahl, P. A. & Darensbourg, M. Y. Effects of sulfur site modification on the redox potentials of derivatives of [N,N′-bis(2-mercaptoethyl)-1,5-diazacyclooctanato]nickel(II). J. Am. Chem. Soc. 115, 4665–4674 (1993).

    Article  CAS  Google Scholar 

  37. Izutsu, K. Acid–Base Dissociation Constants in Dipolar Aprotic Solvents (Blackwell Scientific, 1990).

    Google Scholar 

  38. Costentin, C., Drouet, S., Robert, M. & Savéant, J.-M. Turnover numbers, turnover frequencies, and overpotential in molecular catalysis of electrochemical reactions. Cyclic voltammetry and preparative-scale electrolysis. J. Am. Chem. Soc. 134, 11235–11242 (2012).

    Article  CAS  PubMed  Google Scholar 

  39. Artero, V. & Savéant, J.-M. Toward the rational benchmarking of homogeneous H2-evolving catalysts. Energy Environ. Sci. 7, 3808–3814 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Costentin, C., Dridi, H. & Savéant, J.-M. Molecular catalysis of H2 evolution: diagnosing heterolytic versus homolytic pathways. J. Am. Chem. Soc. 136, 13727–13734 (2014).

    Article  CAS  PubMed  Google Scholar 

  41. Sampson, M. D. & Kubiak, C. P. Electrocatalytic dihydrogen production by an earth-abundant manganese bipyridine catalyst. Inorg. Chem. 54, 6674–6676 (2015).

    Article  CAS  PubMed  Google Scholar 

  42. Shaw, W. J., Helm, M. L. & DuBois, D. L. A modular, energy-based approach to the development of nickel containing molecular electrocatalysts for hydrogen production and oxidation. Biochim. Biophys. Acta Bioenerg. 1827, 1123–1139 (2013).

    Article  CAS  Google Scholar 

  43. Van der Meer, M., Glais, E., Siewert, I. & Sarkar, B. Electrocatalytic dihydrogen production with a robust mesoionic pyridylcarbene cobalt catalyst. Angew. Chem. Int. Ed. 54, 13792–13795 (2015).

    Article  CAS  Google Scholar 

  44. Kampa, M., Pandelia, M.-E., Lubitz, W., van Gastel, M. & Neese, F. A metal–metal bond in the light-induced state of [NiFe] hydrogenases with relevance to hydrogen evolution. J. Am. Chem. Soc. 135, 3915–3925 (2013).

    Article  CAS  PubMed  Google Scholar 

  45. Perotto, C. U. et al. A Ni(I)Fe(II) analogue of the Ni–L state of the active site of the [NiFe] hydrogenases. Chem. Commun. 51, 16988–16991 (2015).

    Article  CAS  Google Scholar 

  46. Yoo, C., Oh, S., Kim, J. & Lee, Y. Transmethylation of a four-coordinate nickel(I) monocarbonyl species with methyl iodide. Chem. Sci. 5, 3853–3858 (2014).

    Article  CAS  Google Scholar 

  47. Greene, B. L., Wu, C.-H., McTernan, P. M., Adams, M. W. W. & Dyer, R. B. Proton-coupled electron transfer dynamics in the catalytic mechanism of a [NiFe]-hydrogenase. J. Am. Chem. Soc. 137, 4558–4566 (2015).

    Article  CAS  PubMed  Google Scholar 

  48. Matson, E. M. et al. Nickel(II) pincer carbene complexes: oxidative addition of an aryl C–H bond to form a Ni(II) hydride. Organometallics 34, 399–407 (2015).

    Article  CAS  Google Scholar 

  49. Breitenfeld, J., Scopelliti, R. & Hu, X. Synthesis, reactivity, and catalytic application of a nickel pincer hydride complex. Organometallics 31, 2128–2136 (2012).

    Article  CAS  Google Scholar 

  50. Boro, B. J., Duesler, E. N., Goldberg, K. I. & Kemp, R. A. Synthesis, characterization, and reactivity of nickel hydride complexes containing 2,6-C6H3(CH2PR2)2 (R = tBu, cHex, and iPr) pincer ligands. Inorg. Chem. 48, 5081 (2009).

    Article  CAS  PubMed  Google Scholar 

  51. Peters, J. W. et al. [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. BBA Mol. Cell Res. 1853, 1350–1369 (2015).

    CAS  Google Scholar 

  52. Adamska, A. et al. Identification and characterization of the ‘super-reduced’ state of the H-cluster in FeFe hydrogenase: a new building block for the catalytic cycle? Angew. Chem. Int. Ed. 51, 11458–11462 (2012).

    Article  CAS  Google Scholar 

  53. Chernev, P. et al. Hydride binding to the active site of [FeFe]-hydrogenase. Inorg. Chem. 53, 12164–12177 (2014).

    Article  CAS  PubMed  Google Scholar 

  54. Ezzaher, S. et al. Evidence for the formation of terminal hydrides by protonation of an asymmetric iron hydrogenase active site mimic. Inorg. Chem. 46, 3426–3428 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. Mealli, C. & Rauchfuss, T. B. Models for the hydrogenases put the focus where it should be—hydrogen. Angew. Chem. Int. Ed. 46, 8942–8944 (2007).

    Article  CAS  Google Scholar 

  56. Barton, B. E., Olsen, M. T. & Rauchfuss, T. B. Aza- and oxadithiolates are probable proton relays in functional models for the FeFe-hydrogenases. J. Am. Chem. Soc. 130, 16834–16835 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Olsen, M. T., Rauchfuss, T. B. & Wilson, S. R. Role of the azadithiolate cofactor in models for FeFe-hydrogenase: novel structures and catalytic implications. J. Am. Chem. Soc. 132, 17733–17740 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Carroll, M. E., Barton, B. E., Rauchfuss, T. B. & Carroll, P. J. Synthetic models for the active site of the FeFe-hydrogenase: catalytic proton reduction and the structure of the doubly protonated intermediate. J. Am. Chem. Soc. 134, 18843–18852 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Zaffaroni, R., Rauchfuss, T. B., Gray, D. L., De Gioia, L. & Zampella, G. Terminal vs bridging hydrides of diiron dithiolates: protonation of Fe2(dithiolate)(CO)2(PMe3)4 . J. Am. Chem. Soc. 134, 19260–19269 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Camara, J. M. & Rauchfuss, T. B. Combining acid–base, redox and substrate binding functionalities to give a complete model for the FeFe-hydrogenase. Nature Chem. 4, 26–30 (2012).

    Article  CAS  Google Scholar 

  61. Reger, D. L. & Coleman, C. Preparation and reactions of the (dicarbonyl) (η5-cyclopentadienyl)(tetrahydrofuran)iron cation: a convenient route to (dicarbonyl)(η5-cyclopentadiemyl)(η2-olefin)iron cations and related complexes. J. Org. Chem. 131, 153–162 (1977).

    Article  CAS  Google Scholar 

  62. Bhugun, I., Lexa, D. & Savéant, J.-M. Homogeneous catalysis of electrochemical hydrogen evolution by iron(0) porphyrins. J. Am. Chem. Soc. 118, 3982–3983 (1996).

    Article  CAS  Google Scholar 

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Acknowledgements

Financial support for this work was provided by Labex arcane (ANR-11-LABX-003), the European Research Council under the European Union's Seventh Framework Programme (FP/2007-2013)/ERC Grant Agreement no. 306398 and the COST Action CM1305 (EcostBio) including an STSM grant (COST-STSM-CM1305- 26539) to D.B.

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Author notes

  1. Trevor R. Simmons

    Present address: Present address: Energy Materials Laboratory, University of East Anglia, Norwich Research Park, Norwich, Norfolk NR4 7TJ, UK,

Authors and Affiliations

  1. Univ. Grenoble Alpes, CNRS UMR 5250, DCM, Grenoble, F-38000, France

    Deborah Brazzolotto, Marcello Gennari & Carole Duboc

  2. Univ. Grenoble Alpes, CNRS UMR 5249, CEA, Laboratoire de Chimie et Biologie des Métaux, Grenoble, F-38000, France

    Deborah Brazzolotto, Nicolas Queyriaux, Trevor R. Simmons & Vincent Artero

  3. Univ. Grenoble Alpes, INAC-LCIB, Grenoble, F-38000, France

    Jacques Pécaut

  4. CEA, DRF-INAC-SyMMES, Reconnaissance Ionique et Chimie de Coordination, Grenoble, F-38000, France

    Jacques Pécaut

  5. Institute of Inorganic Chemistry, Georg-August-University Göttingen, Tammannstrasse 4, Göttingen, D-37077, Germany

    Serhiy Demeshko & Franc Meyer

  6. International Center for Advanced Studies of Energy Conversion (ICASEC), Georg-August-University, Göttingen, D-37077, Germany

    Franc Meyer

  7. Institut des Sciences Moléculaires de Marseille, Aix Marseille Université, CNRS, Centrale Marseille, ISM2 UMR 7313, Marseille, 13397, France

    Maylis Orio

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Contributions

C.D. and V.A. conceived and designed the project. D.B. carried out the experimental work under the supervision of M.G. T.R.S. contributed to the synthetic work. J.P. performed X-ray analysis. F.M. and S.D. performed and analysed the Mössbauer experiments. N.Q. contributed to the analysis of the electrochemical data. M.O. carried out the theoretical calculations. C.D., V.A. and M.G. analysed and interpreted the experimental data and prepared the manuscript. All authors reviewed and contributed to the manuscript.

Corresponding authors

Correspondence to Vincent Artero or Carole Duboc.

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The authors declare no competing financial interests.

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Crystallographic data for compound LN2S2NiIIFeII. (CIF 1725 kb)

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Brazzolotto, D., Gennari, M., Queyriaux, N. et al. Nickel-centred proton reduction catalysis in a model of [NiFe] hydrogenase. Nature Chem 8, 1054–1060 (2016). https://doi.org/10.1038/nchem.2575

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