Maturation of [NiFe]-hydrogenases in Escherichia coli

Biology of Metals - Tập 20 Số 3-4 - 2007
Lucia Forzi1, R. Gary Sawers1
1Max-Planck-Institute for Terrestrial Microbiology, Karl-von-Frisch-Strasse, 35043, Marburg, Germany

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Adams MW (1990) The structure and mechanism of iron-hydrogenases. Biochem Biophys Acta 1020:115–145

Adams MWW, Hall DO (1979) Purification of membrane-bound hydrogenase of Escherichia coli. Biochem J 183:11–22

Andrews SC, Berks BC, McClay J et al (1997) A 12-cistron Escherichia coli operon (hyf) encoding a putative proton-translocating formate hydrogenlyase system. Microbiology 143:3633–3647

Armstrong FA, Albracht SP (2005) [NiFe]-hydrogenases: spectroscopic and electrochemical definition of reactions and intermediates. Philos Trans A Math Phys Eng Sci 363:937–954

Atanassova A, Zamble DB (2005) Escherichia coli HypA is a zinc metalloprotein with a weak affinity for nickel. J Bacteriol 187:4689–4697

Ballantine SP, Boxer DH (1985) Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. J Bacteriol 163:454–459

Ballantine SP, Boxer DH (1986) Isolation and characterisation of a soluble active fragment of hydrogenase isoenzyme 2 from the membranes of anaerobically grown Escherichia coli. Eur J Biochem 156:277–284

Barrett EL, Kwan HS, Macy J (1984) Anaerobiosis, formate, nitrate, and pyrA are involved in the regulation of formate hydrogenlyase in Salmonella typhimurium. J Bacteriol 158:972–977

Blokesch M, Böck A (2002) Maturation of [NiFe]-hydrogenases in Escherichia coli: the HypC cycle. J Mol Biol 324:287–296

Blokesch M, Böck A (2006) Properties of the [NiFe]-hydrogenase maturation protein HypD. FEBS Lett 580:4065–4068

Blokesch M, Magalon A, Böck A (2001) Interplay between the specific chaperone-like proteins HybG and HypC in maturation of hydrogenases 1, 2, and 3 from Escherichia coli. J Bacteriol 183:2817–2822

Blokesch M, Albracht SPJ, Matzanke BF, Drapal N, Böck A (2004a) The complex between hydrogenase-maturation proteins HypC and HypD is an intermediate in the supply of cyanide to the active site iron of [NiFe]-hydrogenases. J Mol Biol 344:155–167

Blokesch M, Paschos A, Bauer A, Reissmann S, Drapal N, Böck A (2004b) Analysis of the transcarbamoylation-dehydration reaction catalyzed by the hydrogenase maturation proteins HypF and HypE. Eur J Biochem 271:3428–3436

Blokesch M, Rohrmoser M, Rode S, Böck A (2004c) HybF, a zinc containing protein involved in NiFe hydrogenase maturation. J Bacteriol 186:2603–2611

Böck A, King PW, Blokesch M, Posewitz MC (2006) Maturation of hydrogenases. Adv Microbiol Physiol 51:1–71

Böhm R, Sauter M, Böck A (1990) Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol 4:231–243

Burgdorf T, Lenz O, Buhrke T et al (2005) [NiFe]-hydrogenases of Ralstonia eutropha H16: Modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 10:181–196

Butland G, Zhang JW, Yang W et al (2006) Interactions of the Escherichia coli hydrogenase biosynthetic proteins: HybG complex formation. FEBS Lett 580:677–681

Cammack R, Frey M, Robson R (2001) Hydrogen as a fuel: learning from nature. Taylor & Francis, London

DerVartanian ME, Menon NK, Pryzbyla AE, Peck HD Jr, DerVartanian DV (1996) Electron paramagnetic resonance (EPR) studies on hydrogenase-1 (HYD1) purified from a mutant strain (AP6) of Escherichia coli enhanced in HYD1. Biochem Biophys Res Commun 227:211–215

Drapal N, Böck A (1998) Interaction of the hydrogenase accessory protein HypC with HycE, the large subunit of Escherichia coli hydrogenase 3 during enzyme maturation. Biochemistry 37:2941–2948

Dubini A, Sargent F (2004) Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Lett 549:141–146

Fritsche E, Paschos A, Beisel HG, Böck A, Huber R (1999) Crystal structure of the hydrogenase maturating endodpeptidase HYBD from Escherichia coli. J Mol Biol 288:989–998

Gasper R, Scrima A, Wittinghofer A (2006) Structural insights into HypB, a GTP-binding protein that regulates metal binding. J Biol Chem 281:27492–27502

Graham A (1981) The organisation of hydrogenase in the cytoplasmic membrane of Escherichia coli. Biochem J 197:283–291

Hedderich R, Forzi L (2005) Energy-converting [NiFe] hydrogenases: more than just H2 activation. J Mol Microbiol Biotechnol 10:92–104

Horner DS, Heil B, Happe T, Embley TM (2002) Iron hydrogenses - ancient enzymes in modern eukaryotes. Trends Biochem Sci 27:148–153

Hube M, Blokesch M, Böck A (2002) Network of hydrogenase maturation in Escherichia coli: role of accessory proteins HypA and HybF. J Bacteriol 184:3879–3885

Jack RL, Buchanan G, Dubini A, Hatzixanthis K, Palmer T, Sargent F (2004) Coordinating assembly and export of complex bacterial proteins. EMBO J 23:3962–3972

Jacobi A, Rossmann R, Böck A (1992) The hyp operon gene products are required for the maturation of catalytically active hydrogenase isoenzymes in Escherichia coli. Arch Microbiol 158:444–451

Jiang J, Acunzo A, Koch SA (2001) Chemistry of [FeII(CN)5(CO)]3-: new observations for a 19th century problem. J Am Chem Soc 123:12109–12110

Leach MR, Sandal S, Sun H, Zamble DB (2005) Metal binding activity of the Escherichia coli hydrogenase maturation factor HypB. Biochemistry 44:12229–12238

Lutz S, Jacobi A, Schlensog V, Böhm B, Sawers G, Böck A (1991) Molecular characterisation of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli. Mol Microbiol 5:123–135

Lyon EJ, Shima S, Boecher R et al (2004a) 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

Lyon EJ, Shima S, Buurmann G, Chowdhuri S et al (2004b) UV-A/blue-light inactivation of the ‘metal-free’ hydrogenase (Hmd) from methanogenic archaea. Eur J Biochem 271:195–204

Magalon A, Böck A (2000a) Analysis of the HypC-HycE complex, a key intermediate in the assembly of the metal center of the Escherichia coli hydrogenase 3. J Biol Chem 275:21114–21220

Magalon A, Böck A (2000b) Dissection of the maturation reactions of the [NiFe] hydrogenase 3 from Escherichia coli taking place after nickel incorporation. FEBS Lett 473:254–258

Maier T, Böck A (1996) Generation of active [NiFe] hydrogenase in vitro from a nickel-free precursor form. Biochemistry 35:10089–10093

Maier T, Jacobi A, Sauter M, Böck A (1993) The product of the hypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J Bacteriol 175:630–635

Maier T, Binder U, Böck A (1996) Analysis of the hydA locus of Escherichia coli: two genes (hydN and hypF) involved in formate and hydrogen metabolism. Arch Microbiol 165:333–341

Mathews RG (1996) One-carbon metabolism. In: Neidhardt FC et al (eds) Escherichia coli and Salmonella: molecular and cellular biology, 2nd edn. ASM Press, pp 600–611

Melis A, Happe T (2001) Hydrogen production: green algae as a source of energy. Plant Physiol 127:740–748

Menon NK, Robbins J, Wendt JC, Shanmugam KT, Przybyla AE (1991) Mutational analysis and characterisation of the Escherichia coli hya operon, which encodes (NiFe) hydrogenase 1. J Bacteriol 173:4851–4861

Menon NK, Chatelus CY, Dervartanian M, Wendt JC, Shanmugam KT, Peck Jr HD, Przybyla AE (1994) Cloning, sequencing, and mutational analysis of the hyb operon encoding Escherichia coli hydrogenase 2. J Bacteriol 176:4416–4423

Nicolet Y, Piras C, Legrand P, Hatchikian EC, Fontecilla-Camps J (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination of an active site Fe binuclear center. Structure 7:13–23

Nicolet Y, Cavazza C, Fontecilla-Camps J (2002) Fe-only hydrogenases: structure, function and evolution. J Inorg Biochem 91:1–8

Palmer T, Sargent F, Berks BC (2005). Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol 13:175–180

Paschos A, Glass RS, Böck A (2001) Carbamoyl phosphate requirement for synthesis of the active center of [NiFe]-hydrogenases. FEBS Lett 488:9–12

Paschos A, Bauer A, Zimmermann A, Zehelein E, Böck A (2002) HypF, a carbamoyl phosphate-converting enzyme involved in [NiFe] hydrogenase maturation. J Biol Chem 277:49945–49951

Peters JW (1999) Structure and mechanism of iron-only hydrogenases. Curr Opin Struct Biol 9:670–676

Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (Cp1) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282:1853–1858

Peters JW, Szilagyi RK, Naumov A, Douglas T (2005) A radical solution for the biosynthesis of the H-cluster of hydrogenase. FEBS Lett 580:363–367

Pickett CJ, Vincent KA, Ibrahim SK et al (2004) Synergic binding of carbon monoxide and cyanide to the FeMo cofactor of nitrogenase: relic chemistry of an ancient enzyme? Chem Eur J 10:4770–4776

Pierik AJ, Hulstein M, Hagen WR, Albracht SPJ (1998) A low-spin iron with CN and CO as intrinsic ligands forms the core of the active site in [Fe]-hydrogenases. Eur J Biochem 258:572–578

Pierik AJ, Roseboom W, Happe RP, Bagley KA, Albracht SPJ (1999) Carbon monoxide and cyanide as intrinsic ligands to iron in the active site of [NiFe]-hydrogenases. J Biol Chem 274:3331–3337

Ragsdale SW (2004) Life with carbon monoxide. Crit Rev Biochem Mol Biol 39:165–195

Reissmann S, Hochleitner E, Wang H et al (2003) Taming of a poison: biosynthesis of the [NiFe]-hydrogenase cyanide ligands. Science 299:1067–1070

Rossmann R, Sawers G, Böck A (1991) Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Mol Microbiol 5:2807–2814

Rossmann R, Sauter M, Lottspeich F, Böck A (1994) Maturation of the large subunit (HycE) of hydrogenase 3 of Escherichia coli requires nickel incorporation followed by C-terminal processing at Arg537. Eur J Biochem 220:377–384

Rossmann R, Maier T, Lottspeich F, Böck A (1995) Characterisation of a protease from Escherichia coli involved in hydrogenase maturation. Eur J Biochem 227:545–550

Roseboom W, Blokesch M, Böck A, Albracht SP (2005) The biosynthetic routes of carbon monoxide and cyanide in the Ni-Fe active site of hydrogenases are different. FEBS Lett 579:469–472

Rubach JK, Brazzolotto X, Gaillard J, Fontecave M (2005) Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima. FEBS Lett 579:5055–5060

Sargent F, Ballantine SP, Rugman PA, Palmer T, Boxer DH (1998) Reassignment of the gene encoding the Escherichia coli hydrogenase 2 small subunit: identification of a soluble precursor of the small subunit in a hypB mutant. Eur J Biochem 255:746–754

Sauter M, Böhm R, Böck A (1992) Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol 6:1523–1532

Sawers RG, Boxer DH (1986) Purification and properties of membrane-bound hydrogenase isoenzyme 1 from anaerobically grown Escherichia coli K12. Eur J Biochem 156:265–275

Sawers RG, Ballantine SP, Boxer DH (1985) Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: evidence for a third isoenzyme. J Bacteriol 164:1324–1331

Sawers RG, Blokesch M, Böck A (2004) Anaerobic formate and hydrogen metabolism. September (2004), posting date. Chapter 3.5.4. In: Curtiss III R (Editor in Chief), EcoSal–Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C. [Online] http://www.ecosal.org

Self WT, Hasona A, Shanmugam KT (2004) Expression and regulation of a silent operon, hyf, coding for hydrogenase 4 isoenzyme in Escherichia coli. J Bacteriol 186:580–587

Skibinski DAG, Golby P, Chang Y-S et al (2002) Regulation of the hydrogenase-4 operon of Escherichia coli by the σ54-dependent transcriptional activators FhlA and HyfR. J Bacteriol 184:6642–6653

Shima S, Lyon EJ, Sordel-Klippert M, Kauß M et al (2004) The cofactor of the iron-sulfur cluster free hydrogenase Hmd: structure of the light-inactivation product. Angew Chemie Int Ed 43:2547–2551

Stephenson M, Stickland LH (1931) Hydrogenase: a bacterial enzyme activating molecular hydrogen. I. The properties of the enzyme. Biochem J 25:205–214

Tard C, Liu XM, Ibrahim SK et al (2005) Synthesis of the H-cluster framework of iron-only hydrogenase. Nature 433:610–613

Tenhunen R, Marver HS, Schmid R (1969) Microsomal heme oxygenase: charaterization of the enzyme. J Biol Chem 244:6388–6294

Thauer RK (1990) Energy metabolism of methanogenic bacteria. Biochim Biophys Acta 1018:256–259

Theodoratou E, Paschos A, Magalon A, Fritsche E, Huber R, Böck A (2000) Nickel serves as substrate recognition motif for the endopeptidase involved in hydrogenase maturation. Eur J Biochem 267:1995–1999

Van der Spek TM, Arendsen AF, Happe RP et al (1996) Similarities in the architecture of the active sites of Ni-hydrogenases and Fe-hydrogenases detected by means of infrared spectroscopy. Eur J Biochem 237:629–634

Vignais PM, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188

Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps J (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373:580–587

Volbeda A, Martin L, Cavazza C et al (2005) Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J Biol Inorg Chem 10:239–249

Waugh R, Boxer DH (1986) Pleiotropic hydrogenase mutants of Escherichia coli K12: growth in the presence of nickel can restore hydrogenase activity. Biochimie 68:157–166

Zalkin H (1997) Formyltetrahydrofolate hydrolase from Escherichia coli. Meth Enzymol 281:214–218

Zhang JW, Butland G, Greenblatt JF, Emili A, Zamble DB (2005) A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J Biol Chem 280:4360–4366

Zinoni F, Birkmann A, Stadtman TC, Böck A (1986) Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. Proc Natl Acad Sci USA 83:4650–4654

Zirngibl C, van Dongen W, Schwörer B et al (1992) H2-forming methylenetetrahydromethanopterin dehydrogenase, a novel type of hydrogenase without iron-sulfur clusters in methanogenic archaea. Eur J Biochem 208:511–520