Reconstitution of [Fe]-hydrogenase using model complexes

Nature Chemistry

Volumn 7, Issue 12, 2015, Pages 995-1002

  Shima, Seigo ^a,b   Chen, Dafa ^c   Xu, Tao ^d   Wodrich, Matthew D ^d   Fujishiro, Takashi ^a   Schultz, Katherine M ^d   Kahnt, Jörg ^a   Ataka, Kenichi ^d,e   Hu, Xile ^d  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c HARBIN INSTITUTE OF TECHNOLOGY   (China)

^d EPFL   (Switzerland)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COENZYME; HYDROGEN; HYDROGENASE; IRON HYDROGENASE; IRON SULFUR PROTEIN; METHENYLTETRAHYDROMETHANOPTERIN; PTERIN DERIVATIVE; PYRIDINE DERIVATIVE;

CHEMICAL STRUCTURE; CHEMISTRY; COENZYME; ENZYME ACTIVE SITE; HYDROGENATION; METABOLISM; THERMODYNAMICS;

CATALYTIC DOMAIN; COENZYMES; HYDROGEN; HYDROGENASE; HYDROGENATION; IRON-SULFUR PROTEINS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PTERINS; PYRIDINES; THERMODYNAMICS;

EID: 84947757387     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.2382     Document Type: Article

References (49)

1. Vignais, P. M., Billoud, B. Occurrence, classification, and biological function of hydrogenases: an overview. Chem. Rev. 107, 4206-4272 (2007).
2. Fontecilla-Camps, J. C., Volbeda, A., Cavazza, C., Nicolet, Y. Structure/function relationships of [NiFe]-and [FeFe]-hydrogenases. Chem. Rev. 107, 4273-4303 (2007).
3. Lubitz, W., Ogata, H., Rudiger, O., Reijerse, E. Hydrogenases. Chem. Rev. 114, 4081-4148 (2014).
4. Shima, S. et al. The crystal structure of [Fe]-hydrogenase reveals the geometry of the active site. Science 321, 572-575 (2008).
5. Shima, S., Ermler, U. Structure and function of [Fe]-hydrogenase and its ironguanylylpyridinol (FeGP) cofactor. Eur. J. Inorg. Chem. 963-972 (2011).
6. Buurman, G., Shima, S., Thauer, R. K. The metal-free hydrogenase from methanogenic archaea: evidence for a bound cofactor. FEBS Lett. 485, 200-204 (2000).
7. Shima, S. et al. The cofactor of the iron-sulfur cluster free hydrogenase Hmd: structure of the light-inactivation product. Angew. Chem. Int. Ed. 43, 2547-2551 (2004).
8. Hiromoto, T. et al. The crystal structure of C176A mutated [Fe]-hydrogenase suggests an acyl-iron ligation in the active site iron complex. FEBS Lett. 583, 585-590 (2009).
9. Vogt, S., Lyon, E. J., Shima, S., Thauer, R. K. The exchange activities of [Fe] hydrogenase (iron-sulfur-cluster-free hydrogenase) from methanogenic archaea in comparison with the exchange activities of [FeFe] and [NiFe] hydrogenases. J. Biol. Inorg. Chem. 13, 97-106 (2008).
10. Hiromoto, T., Warkentin, E., Moll, J., Ermler, U., Shima, S. The crystal structure of an [Fe]-hydrogenase-substrate complex reveals the framework for H2 activation. Angew. Chem. Int. Ed. 48, 6457-6460 (2009).
11. Chen, D., Scopelliti, R., Hu, X. [Fe]-hydrogenase models featuring acylmethylpyridinyl ligands. Angew. Chem. Int. Ed. 49, 7512-7515 (2010).
12. Chen, D., Scopelliti, R., Hu, X. A five-coordinate iron center in the active site of [Fe]-hydrogenase: hints from a model study. Angew. Chem. Int. Ed. 50, 5671-5673 (2011).
13. Hu, B., Chen, D., Hu, X. Synthesis and reactivity of mononuclear iron models of [Fe]-hydrogenase that contain an acylmethylpyridinol ligand. Chem. Eur. J. 20, 1677-1682 (2014).
14. Turrell, P. J., Wright, J. A., Peck, J. N. T., Oganesyan, V. S., Pickett, C. J. The third hydrogenase: a ferracyclic carbamoyl with close structural analogy to the active site of Hmd. Angew. Chem. Int. Ed. 49, 7508-7511 (2010).
15. Schultz, K. M., Chen, D., Hu, X. [Fe]-hydrogenase and models that contain iron-acyl ligation. Chem. Asian J. 8, 1068-1075 (2013).
16. Song, L. C. et al. Synthesis, structural characterization, and some properties of 2-acylmethyl-6-ester group-difunctionalized pyridine-containing iron complexes related to the active site of [Fe]-hydrogenase. Dalton Trans. 43, 8062-8071 (2014).
17. Royer, A. M., Salomone-Stagni, M., Rauchfuss, T. B., Meyer-Klaucke, W. Iron acyl thiolato carbonyls: structural models for the active site of the [Fe]-hydrogenase (Hmd). J. Am. Chem. Soc. 132, 16997-17003 (2010).
18. 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).
19. 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)
20. Ogo, S. et al. A functional [NiFe] hydrogenase mimic that catalyzes electron and hydride transfer from H2. Science 339, 682-684 (2013).
21. Xu, T., Chen, D., Hu, X. Hydrogen-activating models of hydrogenases. Coord. Chem. Rev. 303, 32-41 (2015).
22. Shima, S., Schick, M., Ataka, K., Steinbach, K., Linne, U. Evidence for acyl-iron ligation in the active site of [Fe]-hydrogenase provided by mass spectrometry and infrared spectroscopy. Dalton Trans. 41, 767-771 (2012).
23. Yang, X. Z., Hall, M. B. Monoiron hydrogenase catalysis: hydrogen activation with the formation of a dihydrogen, Fe-H-•••H+-O, bond and methenyl-H4MPT+ triggered hydride transfer. J. Am. Chem. Soc. 131, 10901-10908 (2009).
24. Finkelmann, A. R., Stiebritz, M. T., Reiher, M. Kinetic modeling of hydrogen conversion at [Fe]-hydrogenase active-site models. J. Phys. Chem. B 117, 4806-4817 (2013).
25. Dey, A. Density functional theory calculations on the mononuclear non-heme iron active site of Hmd hydrogenase: role of the internal ligands in tuning external ligand binding and driving H2 heterolysis. J. Am. Chem. Soc. 132, 13892-13901 (2010).
26. Wodrich, M. D., Hu, X. Electronic elements governing the binding of small molecules to a Fe-hydrogenase mimic. Eur. J. Inorg. Chem. 2013, 3993-3999 (2013).
27. Murray, K. A., Wodrich, M. D., Hu, X. L., Corminboeuf, C. Toward functional type III [Fe]-hydrogenase biomimics for H2 activation: insights from computation. Chem.-Eur. J. 21, 3987-3996 (2015).
28. Ma, K., Zirngibl, C., Linder, D., Stetter, K. O., Thauer, R. K. N5,N10-methylenetetrahydromethanopterin dehydrogenase (H2-forming) from the extreme thermophile Methanopyrus kandleri. Arch. Microbiol. 156, 43-48 (1991).
29. Zirngibl, C. et al. H2-forming methylenetetrahydromethanopterin dehydrogenase, a novel type of hydrogenase without iron-sulfur clusters in methanogenic archaea. Eur. J. Biochem. 208, 511-520 (1992).
30. Berggren, G. et al. Biomimetic assembly and activation of [FeFe]-hydrogenases. Nature 499, 66-69 (2013).
31. Esselborn, J. et al. Spontaneous activation of [FeFe]-hydrogenases by an inorganic [2Fe] active site mimic. Nature Chem. Biol. 9, 607-609 (2013).
32. Siebel, J. F. et al. Hybrid [FeFe]-hydrogenases with modified active sites show remarkable residual enzymatic activity. Biochemistry 54, 1474-1483 (2015).
33. Shima, S., Schick, M., Tamura, H. Preparation of [Fe]-hydrogenase from methanogenic archaea. Methods Enzymol. 494, 119-137 (2011).
34. Bart, S. C., Lobkovsky, E., Chirik, P. J. Preparation and molecular and electronic structures of iron(0) dinitrogen and silane complexes and their application to catalytic hydrogenation and hydrosilation. J. Am. Chem. Soc. 126, 13794-13807 (2004).
35. Lagaditis, P. O. et al. Iron(II) complexes containing unsymmetrical P-N-P pincer ligands for the catalytic asymmetric hydrogenation of ketones and imines. J. Am. Chem. Soc. 136, 1367-1380 (2014).
36. Shima, S., Ataka, K. Isocyanides inhibit [Fe]-hydrogenase with very high affinity. FEBS Lett. 585, 353-356 (2011).
37. Lyon, E. J. et al. Carbon monoxide as an intrinsic ligand to iron in the active site of the iron-sulfur-cluster-free hydrogenase H2-forming methylenetetrahydromethanopterin dehydrogenase as revealed by infrared spectroscopy. J. Am. Chem. Soc. 126, 14239-14248 (2004).
38. Korbas, M. et al. The iron-sulfur cluster-free hydrogenase (Hmd) is a metalloenzyme with a novel iron binding motif. J. Biol. Chem. 281, 30804-30813 (2006).
39. Tamura, H. et al. Crystal structures of [Fe]-hydrogenase in complex with inhibitory isocyanides: implications for H2-activation site. Angew. Chem. Int. Ed. 52, 9656-9659 (2013).
40. Finkelmann, A. R., Senn, H. M., Reiher, M. Hydrogen-activation mechanism of [Fe] hydrogenase revealed by multi-scale modeling. Chem. Sci. 5, 4474-4482 (2014).
41. Zhao, Y., Truhlar, D. G. The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals. Theor. Chem. Acc. 120, 215-241 (2008).
42. Zhao, Y., Truhlar, D. G. Density functionals with broad applicability in chemistry. Acc. Chem. Res. 41, 157-167 (2008).
43. Marenich, A. V., Cramer, C. J., Truhlar, D. G. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J. Phys. Chem. B 113, 6378-6396 (2009).
44. Gaussian 09, revision D.01 (Gaussian, Inc., Wallingford, Connecticut, 2009).
45. Steinmann, S. N., Corminboeuf, C. Comprehensive bench marking of a density-dependent dispersion correction. J. Chem. Theory Comp. 7, 3567-3577 (2011).
46. Becke, A. D. Density-functional thermochemistry. 3. The role of exact exchange. J. Chem. Phys. 98, 5648-5652 (1993).
47. Lee, C. T., Yang, W. T., Parr, R. G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron-density. Phys. Rev. B 37, 785-789 (1988).
48. ADF2013 (Scientific Computing and Modelling, Amsterdam, 2013).
49. Klamt, A. The COSMO and COSMO-RS solvation models. WIREs Comput. Mol. Sci. 1, 699-709 (2011).