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Crystal structures of [NiFe] hydrogenase maturation proteins HypC, HypD, and HypE: insights into cyanation reaction by thiol redox signaling.

Watanabe S, Matsumi R, Arai T, Atomi H, Imanaka T, Miki K
Mol Cell 27 29-40 (2007)
Related entries: 2z1c, 2z1e, 2z1f

Cited: 47 times
EuropePMC logo PMID: 17612488

Abstract

[NiFe] hydrogenase maturation proteins HypC, HypD, and HypE catalyze the insertion and cyanation of the iron center of [NiFe] hydrogenases by an unknown mechanism. We have determined the crystal structures of HypC, HypD, and HypE from Thermococcus kodakaraensis KOD1 at 1.8 A, 2.07 A, and 1.55 A resolution, respectively. The structure of HypD reveals its probable iron binding and active sites for cyanation. An extended conformation of each conserved motif of HypC and HypE allows the essential cysteine residues of both proteins to interact with the active site of HypD. Furthermore, the C-terminal tail of HypE is shown to exist in an ATP-dependent dynamic equilibrium between outward and inward conformations. Unexpectedly, the [4Fe-4S] cluster environment of HypD is quite similar to that of ferredoxin:thioredoxin reductase (FTR), indicating the existence of a redox cascade similar to the FTR system. These results suggest a cyanation reaction mechanism via unique thiol redox signaling in the HypCDE complex.

Reviews citing this publication (7)

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Articles citing this publication (40)

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  13. Structure of [NiFe] hydrogenase maturation protein HypE from Escherichia coli and its interaction with HypF. Rangarajan ES, Asinas A, Proteau A, Munger C, Baardsnes J, Iannuzzi P, Matte A, Cygler M. J. Bacteriol. 190 1447-1458 (2008)
  14. [NiFe]-hydrogenase maturation: isolation of a HypC-HypD complex carrying diatomic CO and CN- ligands. Soboh B, Stripp ST, Muhr E, Granich C, Braussemann M, Herzberg M, Heberle J, Gary Sawers R. FEBS Lett. 586 3882-3887 (2012)
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  16. Characterization and in vitro interaction study of a [NiFe] hydrogenase large subunit from the hyperthermophilic archaeon Thermococcus kodakarensis KOD1. Sasaki D, Watanabe S, Kanai T, Atomi H, Imanaka T, Miki K. Biochem. Biophys. Res. Commun. 417 192-196 (2012)
  17. Probing the origin of the metabolic precursor of the CO ligand in the catalytic center of [NiFe] hydrogenase. Bürstel I, Hummel P, Siebert E, Wisitruangsakul N, Zebger I, Friedrich B, Lenz O. J. Biol. Chem. 286 44937-44944 (2011)
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  21. Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation. Sasaki D, Watanabe S, Matsumi R, Shoji T, Yasukochi A, Tagashira K, Fukuda W, Kanai T, Atomi H, Imanaka T, Miki K. J. Mol. Biol. 425 1627-1640 (2013)
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  23. The [NiFe]-hydrogenase accessory chaperones HypC and HybG of Escherichia coli are iron- and carbon dioxide-binding proteins. Soboh B, Stripp ST, Bielak C, Lindenstrauß U, Braussemann M, Javaid M, Hallensleben M, Granich C, Herzberg M, Heberle J, Sawers RG. FEBS Lett. 587 2512-2516 (2013)
  24. Crystal structures of the carbamoylated and cyanated forms of HypE for [NiFe] hydrogenase maturation. Tominaga T, Watanabe S, Matsumi R, Atomi H, Imanaka T, Miki K. Proc. Natl. Acad. Sci. U.S.A. 110 20485-20490 (2013)
  25. The influence of oxygen on [NiFe]-hydrogenase cofactor biosynthesis and how ligation of carbon monoxide precedes cyanation. Stripp ST, Lindenstrauss U, Granich C, Sawers RG, Soboh B. PLoS ONE 9 e107488 (2014)
  26. Dual role of HupF in the biosynthesis of [NiFe] hydrogenase in Rhizobium leguminosarum. Albareda M, Manyani H, Imperial J, Brito B, Ruiz-Argüeso T, Böck A, Palacios JM. BMC Microbiol. 12 256 (2012)
  27. Iron restriction induces preferential down-regulation of H(2)-consuming over H(2)-evolving reactions during fermentative growth of Escherichia coli. Pinske C, Sawers G. BMC Microbiol. 11 196 (2011)
  28. Crystal structure of hydrogenase maturating endopeptidase HycI from Escherichia coli. Kumarevel T, Tanaka T, Bessho Y, Shinkai A, Yokoyama S. Biochem. Biophys. Res. Commun. 389 310-314 (2009)
  29. Identification of an Isothiocyanate on the HypEF Complex Suggests a Route for Efficient Cyanyl-Group Channeling during [NiFe]-Hydrogenase Cofactor Generation. Stripp ST, Lindenstrauss U, Sawers RG, Soboh B. PLoS ONE 10 e0133118 (2015)
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  33. Crystal structures of a [NiFe] hydrogenase large subunit HyhL in an immature state in complex with a Ni chaperone HypA. Kwon S, Watanabe S, Nishitani Y, Kawashima T, Kanai T, Atomi H, Miki K. Proc. Natl. Acad. Sci. U.S.A. 115 7045-7050 (2018)
  34. Maturation of Rhizobium leguminosarum hydrogenase in the presence of oxygen requires the interaction of the chaperone HypC and the scaffolding protein HupK. Albareda M, Pacios LF, Manyani H, Rey L, Brito B, Imperial J, Ruiz-Argüeso T, Palacios JM. J. Biol. Chem. 289 21217-21229 (2014)
  35. A redox-active HybG-HypD scaffold complex is required for optimal ATPase activity during [NiFe]-hydrogenase maturation in Escherichia coli. Haase A, Sawers RG. FEBS Open Bio 13 341-351 (2023)
  36. Electron inventory of the iron-sulfur scaffold complex HypCD essential in [NiFe]-hydrogenase cofactor assembly. Stripp ST, Oltmanns J, Müller CS, Ehrenberg D, Schlesinger R, Heberle J, Adrian L, Schünemann V, Pierik AJ, Soboh B. Biochem J 478 3281-3295 (2021)
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  38. Genome Sequence of a Thermoacidophilic Methanotroph Belonging to the Verrucomicrobiota Phylum from Geothermal Hot Springs in Yellowstone National Park: A Metagenomic Assembly and Reconstruction. Kim HW, Kim NK, Phillips APR, Parker DA, Liu P, Whitaker RJ, Rao CV, Mackie RI. Microorganisms 10 142 (2022)
  39. Structural characterization of HypX responsible for CO biosynthesis in the maturation of NiFe-hydrogenase. Muraki N, Ishii K, Uchiyama S, Itoh SG, Okumura H, Aono S. Commun Biol 2 385 (2019)
  40. The iron-sulfur-containing HypC-HypD scaffold complex of the [NiFe]-hydrogenase maturation machinery is an ATPase. Nutschan K, Golbik RP, Sawers RG. FEBS Open Bio 9 2072-2079 (2019)


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