Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase

Nature

Volumn 479, Issue 7372, 2011, Pages 253-256

  Shomura, Yasuhito ^a,b   Yoon, Ki Seok ^c,e   Nishihara, Hirofumi ^c   Higuchi, Yoshiki ^a,b,d  

^a UNIVERSITY OF HYOGO   (Japan)

^b RIKEN SPring 8 Center ^*  (Japan)

^c IBARAKI UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; CUBANE DERIVATIVE; CYSTEINE; IRON SULFUR PROTEIN; NICKEL IRON HYDROGENASE; OXYGEN; PROTON;

BACTERIUM; CATALYSIS; CLUSTER ANALYSIS; ELECTRON; ENZYME ACTIVITY; IRON; MEMBRANE; OXIDATION; SULFUR;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ELECTRON; ELECTRON TRANSPORT; HYDROGENOVIBRIO MARINUS; MARINE BACTERIUM; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN STRUCTURE;

BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DESULFOVIBRIO GIGAS; HYDROGENASE; IRON; IRON-SULFUR PROTEINS; MODELS, CHEMICAL; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXYGEN; PISCIRICKETTSIACEAE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; PROTONS; STRUCTURE-ACTIVITY RELATIONSHIP; SULFUR;

HYDROGENOVIBRIO MARINUS;

EID: 80855156729     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10504     Document Type: Article

References (37)

1. Vignais, P. M. & Billoud, B. Occurrence, classification, and biological function of hydrogenases: an overview. Chem. Rev. 107, 4206-4272 (2007). (Pubitemid 350041744)
2. Vincent, K. A. et al. Electrocatalytic hydrogen oxidation by an enzyme at high carbon monoxide or oxygen levels. Proc. Natl Acad. Sci. USA 102, 16951-16954 (2005). (Pubitemid 41692664)
3. Luo, X., Brugna, M., Tron-Infossi, P., Giudici-Orticoni, M. T. & Lojou, E. Immobilization of the hyperthermophilic hydrogenase from Aquifex aeolicus bacterium onto gold and carbon nanotube electrodes for efficient H2 oxidation. J. Biol. Inorg. Chem. 14, 1275-1288 (2009).
4. Lukey, M. J. et al. How Escherichia coli is equipped to oxidize hydrogen under different redox conditions. J. Biol. Chem. 285, 3928-3938 (2010).
5. De Lacey, A. L., Fernandez, V. M., Rousset, M. & Cammack, R. Activation and inactivation of hydrogenase function and the catalytic cycle: spectroelectrochemical studies. Chem. Rev. 107, 4304-4330 (2007). (Pubitemid 350041746)
6. Brugna-Guiral, M. et al. [NiFe] hydrogenases from the hyperthermophilic bacteriumAquifex aeolicus: properties, function, and phylogenetics. Extremophiles 7, 145-157 (2003).
7. Burgdorf, T. et al. [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J. Mol. Microbiol. Biotechnol. 10, 181-196 (2005). (Pubitemid 43800692)
8. Yoon, K.-S., Fukuda, K., Fujisawa, K. & Nishihara, H. Purification and characterization of a highly thermostable, oxygen-resistant, respiratory [NiFe]-hydrogenase from a marine, aerobic hydrogen-oxidizing bacterium Hydrogenovibrio marinus. Int. J. Hydrogen Energy 36, 7081-7088 (2011).
9. Volbeda,A. et al. Crystal structure of the nickel-ironhydrogenase fromDesulfovibrio gigas. Nature 373, 580-587 (1995).
10. Higuchi, Y., Yagi, T. & Yasuoka, N. Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 5, 1671-1680 (1997). (Pubitemid 28051979)
11. Montet, Y. et al. Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics. Nature Struct. Biol. 4, 523-526 (1997). (Pubitemid 127742473)
12. Matias, P. M. et al. [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8A and modelling studies of its interaction with the tetrahaem cytochrome c3. J. Biol. Inorg. Chem. 6, 63-81 (2001). (Pubitemid 32822158)
13. Fontecilla-Camps, J. C., Volbeda, A., Cavazza, C. & Nicolet, Y. Structure/function relationships of [NiFe]-and [FeFe]-hydrogenases. Chem. Rev. 107, 4273-4303 (2007).
14. Saggu, M. et al. Spectroscopic insights into the oxygen-tolerant membraneassociated [NiFe] hydrogenase of Ralstonia eutropha H16. J. Biol. Chem. 284, 16264-16276 (2009).
15. Peters, J. W. et al. Redox-dependent structural changes in the nitrogenase P-cluster. Biochemistry 36, 1181-1187 (1997). (Pubitemid 27074941)
16. Berrisford, J. M. & Sazanov, L. A. Structural basis for the mechanismof respiratory complex I. J. Biol. Chem. 284, 29773-29783 (2009).
17. Aragão, D., Mitchell, E. P., Frazao, C. F., Carrondo, M. A.&Lindley, P. F. Structural and functional relationships in the hybrid cluster protein family: structure of the anaerobically purified hybrid cluster protein from Desulfovibrio vulgaris at 1.35A resolution. Acta Crystallogr. D 64, 665-674 (2008). (Pubitemid 351872068)
18. Huang, W. et al. Crystal structure of nitrile hydratase reveals a novel iron centre in a novel fold. Structure 5, 691-699 (1997). (Pubitemid 27236267)
19. Pandelia, M. E. et al. Characterization of a unique [FeS] cluster in the electron transfer chain of the oxygen tolerant [NiFe] hydrogenase from Aquifex aeolicus. Proc. Natl Acad. Sci. USA 108, 6097-6102 (2011).
20. Schneider, K., Patil, D. S. & Cammack, R. ESR properties of membrane-bound hydrogenase from aerobic hydrogen bacteria. Biochim. Biophys. Acta 748, 353-361 (1983).
21. Knü ttel, K. et al. Redox properties of the metal centres in the membrane-bound hydrogenase from Alcaligenes eutrophus CH34. Bull. Pol. Acad. Sci. Chem. 42, 495-511 (1994).
22. Goris, T. et al.A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Nature Chem. Biol. 7, 310-318 (2011).
23. Dementin, S. et al. A glutamate is the essential proton transfer gate during the catalytic cycle of the [NiFe] hydrogenase. J. Biol. Chem. 279, 10508-10513 (2004). (Pubitemid 38372661)
24. Teixeira, V. H., Soares, C. M. & Baptista, A. M. Proton pathways in a [NiFe]-hydrogenase: A theoretical study. Proteins 70, 1010-1022 (2008). (Pubitemid 351161957)
25. Lubitz, W., Reijerse, E. & van Gastel, M. [NiFe] and [FeFe] hydrogenases studied by advanced magnetic resonance techniques. Chem. Rev. 107, 4331-4365 (2007). (Pubitemid 350041747)
26. Fernandez, V. M., Hatchikian, E. C., Patil, D. S.&Cammack, R. ESR-detectable nickel and iron-sulphur centres in relation to the reversible activation of Desulfovibrio gigas hydrogenase. Biochim. Biophys. Acta 883, 145-154 (1986).
27. Cracknell, J. A., Wait, A. F., Lenz, O., Friedrich, B. & Armstrong, F. A. A kinetic and thermodynamic understanding ofO2 tolerance in [NiFe]-hydrogenases. Proc.Natl Acad. Sci. USA 106, 20681-20686 (2009).
28. Marques, M. C., Coelho, R., De Lacey, A. L., Pereira, I. A. & Matias, P. M. The threedimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough: a hydrogenase without a bridging ligand in the active site in its oxidised, "as-isolated" state. J. Mol. Biol. 396, 893-907 (2010).
29. Buhrke, T., Lenz, O., Krauss, N. & Friedrich, B. Oxygen tolerance of the H2-sensing [NiFe] hydrogenase from Ralstonia eutropha H16 is based on limited access of oxygen to the active site. J. Biol. Chem. 280, 23791-23796 (2005). (Pubitemid 40884864)
30. Duché, O., Elsen, S., Cournac, L. & Colbeau, A. Enlarging the gas access channel to the active site renders the regulatory hydrogenase HupUV of Rhodobacter capsulatus O2 sensitive without affecting its transductory activity. FEBS J. 272, 3899-3908 (2005). (Pubitemid 41117221)
31. Shomura, Y., Hagiya, K., Yoon, K.-S., Nishihara, H. & Higuchi, Y. Crystallization and preliminary X-ray diffraction analysis of membrane-bound respiratory [NiFe] hydrogenase fromHydrogenovibriomarinus.Acta Crystallogr. F67,827-829(2011).
32. Ueno, G., Kanda, H.,Kumasaka, T.&Yamamoto, M.Beamline Scheduling Software: administration software for automatic operation of the RIKENstructural genomics beamlines at SPring-8. J. Synchrotron Radiat. 12, 380-384 (2005). (Pubitemid 41557615)
33. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
34. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
35. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255 (1997). (Pubitemid 27235885)
36. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004). (Pubitemid 41742764)