Abstract
Escherichia coli has the capacity to synthesise three distinct formate dehydrogenase isoenzymes and three hydrogenase isoenzymes. All six are multisubunit, membrane-associated proteins that are functional in the anaerobic metabolism of the organism. One of the formate dehydrogenase isoenzymes is also synthesised in aerobic cells. Two of the formate dehydrogenase enzymes and two hydrogenases have a respiratory function while the formate dehydrogenase and hydrogenase associated with the formate hydrogenlyase pathway are not involved in energy conservation. The three formate dehydrogenases are molybdo-selenoproteins while the three hydrogenases are nickel enzymes; all six enzymes have an abundance of iron-sulfur clusters. These metal requirements alone invoke the necessity for a profusion of ancillary enzymes which are involved in the preparation and incorporation of these cofactors. The characterisation of a large number of pleiotropic mutants unable to synthesise either functionally active formate dehydrogenases or hydrogenases has led to the identification of a number of these enzymes. However, it is apparent that there are many more accessory proteins involved in the biosynthesis of these isoenzymes than originally anticipated. The biochemical function of the vast majority of these enzymes is not understood. Nevertheless, through the construction and study of defined mutants, together with sequence comparisons with homologous proteins from other organisms, it has been possible at least to categorise them with regard to a general requirement for the biosynthesis of all three isoenzymes or whether they have a specific function in the assembly of a particular enzyme. The identification of the structural genes encoding the formate dehydrogenase and hydrogenase isoenzymes has enabled a detailed dissection of how their expression is coordinated to the metabolic requirement for their products. Slowly, a picture is emerging of the extremely complex and involved path of events leading to the regulated synthesis, processing and assembly of catalytically active formate dehydrogenase and hydrogenase isoenzymes. This article aims to review the current state of knowledge regarding the biochemistry, genetics, molecular biology and physiology of these enzymes.
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Abou-Jaoude A, Chippaux M & Pascal M-C (1979a) Formate-nitrite reduction inEscherichia coli K12: physiological study of the system. Eur. J. Biochem. 95: 309–314
Abou-Jaoude A, Pascal M-C & Chippaux M (1979b) Formate-nitrite reduction inEscherichia coli K12: identification of components involved in the electron transfer. Eur. J. Biochem. 95: 315–321
Ackrell BAC, Asato RN & Mower HF (1966) Multiple forms of bacterial hydrogenase. J. Bacteriol. 92: 828–838
Adams MWW & Hall DO (1979) Purification of membrane-bound hydrogenase ofEscherichia coli. Biochem. J. 183: 11–22
Albracht SPJ, Graf E-G & Thauer RK (1982) The EPR properties of nickel in hydrogenase fromMethanobacterium thermoautotrophicum. FEBS Lett. 140: 311–313
Anraku Y & Gennis RB (1987) The aerobic respiratory chains ofEscherichia coli. Trends Biochem. Sci. 12: 262–266
Axley MJ, Böck A & Stadtman TC (1991) Catalytic properties of anEscherichia coli formate dehydrogenase mutant in which sulfur replaces selenium. Proc. Natl. Acad. Sci. USA 88: 8450–8454
Axley MJ & Grahame DA (1991) Kinetics of formate dehydrogenase ofEscherichia coli formate-hydrogenlyase. J. Biol. Chem. 266: 13731–13736
Axley MJ, Grahame DA & Stadtman TC (1990)Escherichia coli formate-hydrogen lyase: purification and properties of the selenium-dependent formate dehydrogenase component. J. Biol. Chem. 265: 18213–18218
Azoulay E, Giordano G, Grillet L, Rosset R & Haddock BA (1978) Properties ofEscherichia coli K-12 mutants that are sensitive to chlorate when grown aerobically. FEMS Microbiol. Lett. 4: 235–240
Baker KP & Boxer DH (1991) Regulation of thechlA locus ofEscherichia coli K12: involvement of molybdenum cofactor. Mol. Microbiol. 5: 901–908
Ballantine SP & Boxer DH (1985) Nickel-containing hydrogenase isoenzymes from anaerobically grownEscherichia 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 grownEscherichia coli. Eur. J. Biochem. 156: 277–284
Barrett EL, Jackson CE, Fukumoto HT & Chang GW (1979) Formate dehydrogenase mutants ofSalmonella typhimurium: a new medium for their isolation and new mutant classes. Mol. Gen. Genet. 177: 95–101
Barrett EL & Riggs DL (1982)Salmonella typhimurium mutants defective in the formate dehydrogenase linked to nitrate reductase. J. Bacteriol. 149: 554–560
Belaich A & Belaich JP (1976) Microcalorimetric study of the anaerobic growth ofEscherichia coli: growth thermograms in a synthetic medium. J. Bacteriol. 125: 14–18
Berg BL, Baron C & Stewart V (1991a) Nitrate-inducible formate dehydrogenase inEscherichia coli K-12: evidence that a mRNA stem-loop structure is essential for decoding opal (UGA) as selenocysteine. J. Biol. Chem. 266: 22386–22391
Berg BL, Li J, Heider J & Stewart V (1991b) Nitrate-inducible formate dehydrogenase inEscherichia coli K-12: nucleotide sequence of thefdnGHI operon and evidence that opal (UGA) encodes selenocysteine. J. Biol. Chem. 266: 22380–22385
Berg BL & Stewart V (1990) Structural genes for nitrate-inducible formate dehydrogenase inEscherichia coli K-12. Genetics 125: 691–702
Bernhard T & Gottschalk G (1978a) The hydrogenase ofEscherichia coli, purification, some properties and the function of the enzyme. In: Schlegel HG & Schneider K (Eds) Hydrogenases: Their Catalytic Activity, Structure and Function (pp 199–208). E. Goltze KG, Göttingen
Bernhard T & Gottschalk G (1978b) Cell yields ofEscherichia coli during anaerobic growth on fumarate and molecular hydrogen. Arch. Microbiol. 116: 235–238
Bilous PT, Cole ST, Anderson WF & Weiner JH (1988) Nucleotide sequence of thedmsABC operon encoding the anaerobic dimethylsulfoxide reductase ofEscherichia coli. Mol. Microbiol. 2: 785–795
Birkmann A & Böck A (1989) Characterisation of acis regulatory DNA element necessary for formate induction of the formate dehydrogenase gene (fdhF) ofEscherichia coli. Mol. Microbiol. 3: 187–195
Birkmann A, Hennecke H & Böck A (1989) Construction of chimaeric promoter regions by exchange of the upstream regulatory sequences fromfdhF andnif genes. Mol. Microbiol. 3: 697–703
Birkmann A, Sawers RG & Böck A (1987a) Involvement of thentrA gene product in the anaerobic metabolism ofEscherichia coli. Mol. Gen. Genet. 210: 535–542
Birkmann A, Zioni F, Sawers G & Böck A (1987b) Factors affecting transcriptional regulation of the formate-hydrogen-lyasepathway ofEscherichia coli. Arch. Microbiol. 148: 44–51
Blasco F, Iobbi C, Giordano G, Chippaux M & Bonnefoy V (1989) Nitrate reductase ofEscherichia coli: completion of the nucleotide sequence of thenar operon and reassessment of the role of the α and β subunits in iron binding and electron transfer. Mol. Gen. Genet. 218: 249–257
Böck A, Forchhammer K, Heider H & Baron C (1991a) Selenoprotein synthesis: an expansion of the genetic code. Trends Biochem. Sci. 16: 463–467
Böck A, Forchhammer K, Heider J, Leinfelder W, Sawers G, Veprek B & Zinoni F (1991b) Selenocysteine: the 21st amino acid. Mol. Microbiol. 5: 515–520
Böhm R, Sauter M & Böck A (1990) Nucleotide sequence and expression of an operon inEscherichia coli coding for formate hydrogenlyase components. Mol. Microbiol. 4: 231–243
Bokranz M, Gutmann M, Körtner C, Kojro E, Fahrenholz F, Lauterbach F & Kröger A (1991) Cloning and nucleotide sequence of the structural genes encoding the formate dehydrogenase ofWolinella succinogenes. Arch. Microbiol. 156: 119–128
Boone-Miller J, Scott DJ & Amy NK (1987) Molybdenum-sensitive transcriptional regulation of thechlD locus ofEscherichia coli. J. Bacteriol. 169: 1853–1860
Bourne HR, Sanders DA & McCormick F (1991) The GTPase super family: conserved structure and molecular mechanism. Nature (London) 349: 117–127
Brown TA & Shrift A (1982) Selective assimilation of selenite byEscherichia coli. Can. J. Microbiol. 28: 307–310
Chaudhuri A & Krasna AI (1987) Isolation of genes required for hydrogenase synthesis inEscherichia coli. J. Gen. Microbiol. 133: 3289–3298
Chiang RC, Cavicchioli R & Gunsalus RP (1992) Identification and characterisation ofnarQ, a second nitrate sensor for nitrate-dependent gene regulation inEscherichia coli. Mol. Microbiol. 6: 1913–1923
Chippaux M, Pascal M-C & Casse F (1977) Formate hydrogenlyase system inSalmonella typhimurium LT2. Eur. J. Biochem. 72: 149–155
Colbeau A, Magnin JP, Cauvin B, Champion T & Vignais PM (1993) Organisation of the genes necessary for hydrogenase expression inRhodobacter capsulatus. Sequence analysis and identification of twohyp regulatory mutants. Mol. Microbiol. 8: 15–29
Cole JA & Wimpenny JWT (1966) The inter-relationships of low redox potential cytochromec 552 and hydrogenase in facultative anaerobes. Biochim. Biophys. Acta 128: 419–425
Corcuera GL, Bastidas M & Dubourdieu M (1993) Molybdenum uptake inEscherichia coli K12. J. Gen. Microbiol. 139: 1869–1875
Cotter PG & Gunsalus RP (1992) Contribution of thefnr andarcA gene products in coordinate regulation of cytochromeo andd oxidase (cyoABCDE andcydAB) genes inEscherichia coli. FEMS Microbiol. Lett. 91: 31–36
Cox JC, Edwards ES & DeMoss JA (1981) Resolution of distinct selenium-containing formate dehydrogenases fromEscherichia coli. J. Bacteriol. 145: 1317–1324
Darwin A, Hussain H, Griffiths L, Grove J, Sambongi Y, Busby S & Cole J (1993a) Regulation and sequence of the structural gene for cytochromec 552 fromEscherichia coli: not a hexahaem but a 50 kDa tetrahaem nitrite reductase. Mol. Microbiol. 9: 1255–1266
Darwin A, Tormay P, Page L, Griffiths L & Cole J (1993b) Identification of the formate dehydrogenases and genetic determinants of formate-dependent nitrite reduction byEscherichia coli K12. J. Gen. Microbiol. 139: 1829–1840
DeMoss JA & Hsu P-Y (1991)NarK enhances nitrate uptake and nitrite excretion inEscherichia coli. J. Bacteriol. 173: 3303–3310
Dross F, Geisler V, Lenger R, Theis F, Kraft T, Fahrenholz F, Kojro E, Duchene A, Tripier D, Juvenal K & Kröger A (1992) The quinone-reactive Ni/Fe-hydrogenase ofWolinella succinogenes. Eur. J. Biochem. 206: 93–102
Ehrenreich A, Forchhammer K, Tormay P, Veprek B & Böck A (1992) Selenoprotein synthesis inE. coli: purification and characterisation of the enzyme catalysing selenium activation. Eur. J. Biochem. 206: 767–773
Eidsness MK, Scott RA, Pickril B, DerVartanian DV, LeGall J, Moura I, Moura JJG & Peck HD (1989) Evidence for selenocysteine coordination to the active site nickel in the (NiFeSe) hydrogenase fromDesulfovibrio baculatus. Proc. Natl. Acad. Sci. USA 86: 147–151
Eitinger T & B Friedrich (1991) Cloning, nucleotide sequence and heterologous expression of a high affinity nickel transport gene fromAlcaligenes eutrophus. J. Biol. Chem. 266: 3222–3227
Enoch HG & Lester RL (1974) The role of a novel cytochromeb-containing nitrate reductase and quinone in thein vitro reconstruction of formate-nitrate reductase activity ofE. coli. Biochem. Biophys. Res. Commun. 61: 1234–1241
Enoch HG & Lester RL (1975) The purification and properties of formate dehydrogenase and nitrate reductase fromEscherichia coli. J. Biol. Chem. 250: 6693–6705
Forchhammer K, Boesmiller K & Böck A (1991a) The function of selenocysteine synthase and SELB in the synthesis and incorporation of selenocysteine. Biochimie 73: 1481–1486
Forchhammer K, Leinfelder W & Böck A (1989) Identification of a novel translation factor necessary for the incorporation of selenocysteine into protein. Nature (London) 342: 453–456
Forchhammer K, Leinfelder W, Boesmiller K, Veprek B & Böck A (1991b) Selenocysteine synthase fromEscherichia coli: nucleotide sequence of the gene (selA) and purification of the protein. J. Biol. Chem. 266: 6318–6323
Francis K, Patel P, Wendt JC & Shanmugam KT (1990) Purification and characterisation of two forms of hydrogenase isoenzyme 1 fromEscherichia coli. J. Bacteriol. 172: 5750–5757
Freundlich M, Ramani N, Mathew E, Sirko A & Tsui P (1992) The role of integration host factor in gene expression inEscherichia coli. Mol. Microbiol. 6: 2557–2563
Friedrich B & Schwarz E (1993) Molecular biology of hydrogen utilisation in aerobic chemolithotrophs. Annu. Rev. Microbiol. 47: 351–383
Fujita T & Sato R (1967) Nitrite-dependent gas evolution in cells containing cytochromec 552. J. Biochem. (Tokyo) 62: 230–238
Fukuyama T & Ordal EJ (1965) Induced biosynthesis of formic hydrogenlyase in iron-deficient cells ofEscherichia coli. J. Bacteriol. 90: 673–680
Garland PB, Downie JA & Haddock BA (1975) Proton translocation and the respiratory nitrate reductase ofEscherichia coli. Biochem. J. 152: 547–559
Gest H & Peck HD (1955) A study of the hydrogenlyase reaction with systems derived from normal and anaerogenic coliaerogenes bacteria. J. Bacteriol. 70: 326–334
Giordano G, Medani C-L, Mandrand-Berthelot M-A & Boxer DH (1983) Formate dehydrogenase fromEscherichia coli. FEMS Microbiol. Lett. 17: 171–177
Glick BR, Wang PY, Schneider H & Martin WG (1980) Identification and partial characterisation of anEscherichia coli mutant with altered hydrogenase activity. Can. J. Biochem. 58: 361–367
Glick BR, Zeisler J, Banazuk AM, Friesen JD & Martin WG (1981) The identification and partial characterisation of a plasmid containing the gene for the membrane-associated hydrogenase fromE. coli. Gene 15: 201–206
Graf E-G & Thauer RK (1981) Hydrogenase fromMethanobacterium thermoautotrophicum: a nickel-containing enzyme. FEBS Lett. 136: 165–169
Graham A (1981) The organisation of hydrogenase in the cytoplasmic membrane ofEscherichia coli. Biochem. J. 197: 283–291
Graham A & Boxer DH (1981) The organisation of formate dehydrogenase in the cytoplasmic membrane ofEscherichia coli. Biochem. J. 195: 627–637
Graham A, Boxer DH, Haddock BA, Mandrand-Berthelot M-A & Jones RW (1980) Immunological analysis of the membrane-bound hydrogenase ofEscherichia coli. FEBS Lett. 113: 167–172
Green J, Trageser M, Six S, Unden G & Guest JR (1991) Characterisation of the FNR protein ofEscherichia coli, an iron-binding transcriptional regulator. Proc. R. Soc. London 244: 137–144
Guest JR (1992) Oxygen-regulated gene expression inEscherichia coli. J. Gen. Microbiol. 138: 2253–2263
Gunsalus RP (1992) Control of electron flow inEscherichia coli: coordinated transcription of respiratory pathway genes. J. Bacteriol. 174: 7069–7074
Haddock BA & Jones CW (1977) Bacterial respiration. Bacteriol. Rev. 41: 47–99
Haddock BA & Mandrand-Berthelot M-A (1982)Escherichia coli formate-to-nitrate respiratory chain: genetic analysis. Biochem. Soc. Trans. 10: 478–480
Hallahan DL, Fernandez VM & Hall DO (1987) Reversible activation of hydrogenase fromEscherichia coli. Eur. J. Biochem. 165: 621–625
He S-H, Teixeira M, LeGall J, Patil DS, DerVartanian DV, Huynh BH & Peck HD (1989) EPR studies with77Se enriched (NiFeSe) hydrogenase ofDesulfovibrio baculatus. Evidence for a selenium ligand to the active-site nickel. J. Biol. Chem. 264: 2678–2682
Heider J & Böck A (1993) Selenium metabolism in micro-organisms. Adv. Microbial Physiol. 35: 71–109
Higgins CF, Gallacher MP, Hyde SC, Mimmack ML & Pearce SR (1990) Periplasmic binding protein-dependent transport systems: the membrane associated components. Phil. Trans. R. Soc. London 326: 353–365
Hopper S, Babst M, Schlensog V, Fischer H-M, Hennecke H & Böck A (1994) Regulated expressionin vitro of genes coding for formate hydrogenlyase components ofEscherichia coli. J. Biol. Chem. in press
Itagaki E, Fujita T & Sato R (1961) Cytochromeb 1-nitrate reductase interaction in a solubilised system fromEscherichia coli. Biochim. Biophys. Acta 51: 390–392
Itagaki E, Fujita T & Sato R (1962) Solubilisation and properties of formate dehydrogenase and cytochromeb 1 fromEscherichia coli. J. Biochem. (Tokyo) 52: 131–141
Iuchi S & Lin ECC (1987) ThenarL gene product activates the nitrate reductase operon and represses the fumarate reductase and trimethylamineN-oxide reductase operons inEscherichia coli. Proc. Natl. Acad. Sci. USA 84: 3901–3905
Iuchi S & Lin ECC (1991) Adaptation ofEscherichia coli to respiratory conditions: regulation of gene expression. Cell 66: 5–7
Iuchi S & Lin ECC (1993) Adaptation ofEscherichia coli to redox environments by gene expression. Mol. Microbiol. 9: 9–15
Jacobi A, Rossmann R & Böck A (1992) Thehyp operon gene products are required for the maturation of catalytically active hydrogenase isoenzymes inEscherichia coli. Arch. Microbiol. 158: 444–451
Jamieson DJ, Sawers RG, Rugman PA, Boxer DH & Higgins CF (1986) Effects of anaerobic regulatory mutations and catabolite repression on regulation of hydrogen metabolism and hydrogenase isoenzyme composition inSalmonella typhimurium. J. Bacteriol. 168: 405–411
Jasper P & Silver S (1977) Magnesium transport in microorganisms, In: Weinberg ED (Ed) Microorganisms and Minerals (pp 7–74). Marcel Dekker, New York
Johann S & Hinton SM (1987) Cloning and nucleotide sequence of thechlD locus. J. Bacteriol. 169: 1911–1916
Johnson JL, Bastian NR & Rajagopalan KV (1990) Molybdenum guanine dinucleotide: a modified form of molybdopterin identified in the molybdenum cofactor of dimethlsulfoxide reductase fromRhodobacter sphaeroides forma specialisdenitrificans. Proc. Natl. Acad. Sci. USA 87: 3190–3194
Johnson JL, Indermaur LW & Rajagopalan KV (1991) Molybdenum cofactor biosynthesis inEscherichia coli. J. Biol. Chem. 266: 12140–12145
Jones RW (1980a) Proton translocation by the membrane-bound formate dehydrogenase ofEscherichia coli. FEMS Microbiol. Lett. 8: 167–171
Jones RW (1980b) The role of the membrane-bound hydrogenase in the energy-conserving oxidation of molecular hydrogen byEscherichia coli. Biochem. J. 188: 345–350
Jones RW & Garland PB (1977) Sites and specificity of the reaction of bipyridylium compounds with anaerobic respiratory enzymes ofEscherichia coli: effects of permeability barriers imposed by the cytoplasmic membrane. Biochem. J. 164: 199–211
Jones RW, Lamont A & Garland PB (1980) The mechanism of proton translocation driven by the respiratory nitrate reductase complex ofEscherichia coli. Biochem. J. 190: 79–94
Kalman L & Gunsalus RP (1988) ThefrdR gene ofEscherichia coli globally regulates several operons involved in anaerobic growth in response to nitrate. J. Bacteriol. 170: 623–629
Karube I, Tomiyama M & Kikuchi A (1984) Molecular cloning and physical mapping of thehyd gene ofEscherichia coli K-12. FEMS Microbiol. Lett. 25: 165–168
Kessler D, Herth W & Knappe J (1992) Ultrastructure and pyruvateformate-lyase quenching property of the multienzymic AdhE protein ofEscherichia coli. J. Biol. Chem. 267: 18073–18079
Knappe J, Neugebauer FA, Blaschkowski HP & Gänzler M (1984) Post-translational activation introduces a free radical into pyruvate formate-lyase. Proc. Natl. Acad. Sci. USA 81: 1332–1335
Knappe J & Sawers G (1990) A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system ofEscherichia coli. FEMS Microbiol. Rev. 75: 383–398
Kohara Y, Akiyama K & Isono K (1987) The physical map of the wholeE. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell 50: 495–508
Kramer GF & Ames BN (1988) Isolation and characterisation of a selenium metabolism mutant ofSalmonella typhimurium. J. Bacteriol. 170: 736–743
Krasna AI (1984) Mutants ofEscherichia coli with altered hydrogenase activity. J. Gen. Microbiol. 130: 779–787
Lambden PR & Guest JR (1976) Mutants ofEscherichia coli K-12 unable to use fumarate as an anaerobic electron acceptor. J. Gen. Microbiol. 97: 145–160
Lee JH, Patel P, Sankar P & Shanmugam KT (1985) Isolation and characterisation of mutant strains ofEscherichia coli altered in hydrogen metabolism. J. Bacteriol. 162: 344–352
Lee JH, Wendt JC & Shanmugam KT (1990) Identification of new gene,molR, essential for the utilisation of molybdate byEscherichia coli. J. Bacteriol. 172: 2079–2087
Leinfelder W, Forchhammer K, Veprek B, Zehelein E & Böck A (1990)In vitro synthesis of selenocysteinyl-tRNA U C A from seryl-tRNA U C A : involvement and characterisation of theselD gene product. Proc. Natl. Acad. Sci. USA 87: 543–547
Leinfelder W, Forchhammer K, Zinoni F, Sawers G, Mandrand-Bertheolt M-A & Böck A (1988a)Escherichia coli genes whose products are involved in selenium metabolism. J. Bacteriol. 170: 540–546
Leinfelder W, Zehelein E, Mandrand-Berthelot M-A & Böck A (1988b) Gene for a novel tRNA species that accepts L-serine and cotranslationally inserts selenocysteine. Nature (London) 331: 723–725
Lester RL & DeMoss JA (1971) Effects of molybdate and selenite on formate and nitrate metabolism inEscherichia coli. J. Bacteriol. 105: 1006–1014
Li J & Stewart V (1992) Localisation of upstream sequence elements required for nitrate and anaerobic induction offdn (formate dehydrogenase-N) operon expression inEscherichia coli K-12. J. Bacteriol. 174: 4935–4942
Lutz S, Böhm R, Beier A & Böck A (1990) Characterisation of divergent NtrA-dependent promoters in the anaerobically expressed gene cluster coding for hydrogenase 3 components ofEscherichia coli. Mol. Microbiol. 4: 13–20
Lutz S, Jacobi A, Schlensog V, Böhm R, Sawers G & Böck A (1991) Molecular characterisation of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes inEscherichia coli. Mol. Microbiol. 5: 123–135
Macy J, Kulla H & Gottschalk G (1976) Hydrogen-dependent anaerobic growth ofEscherichia coli on L-malate: succinate formation. J. Bacteriol. 125: 423–428
Maier T, Jacobi A, Sauter M & Böck A (1993) The product of thehypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J. Bacteriol. 175: 630–635
Mandrand-Berthelot M-A, Couchoux-Luthaud G, Santini C-L & Giordano G (1988) Mutants ofEscherichia coli specifically defective in respiratory formate dehydrogenase activity. J. Gen. Microbiol. 134: 3129–3139
Mandrand-Berthelot MA, Wee MKK & Haddock BA (1978) An improved method for identification and characterization of mutants ofEscherichia coli deficient in formate dehydrogenase activity. FEMS Microbiol. Lett. 4: 37–40
Maupin JA & Shanmugam KT (1990) Genetic regulation of formate hydrogenlyase ofEscherichia coli: role of thefhlA gene product as a transcriptional activator for a new regulatory gene,fhlB. J. Bacteriol. 172: 4798–4806
Menon NK, Robbins J, Peck HD, Chatelus CY, Choi E-S & Przybyla AE (1990) Cloning and sequencing of a putativeEscherichia coli (NiFe) hydrogenase-1 operon containing six open reading frames. J. Bacteriol. 172: 1969–1977
Menon NK, Robbins J, Wendt JC, Shanmugam KT & Przybyla AE (1991) Mutational analysis and characterisation of theEscherichia coli hya operon, which encodes (NiFe) hydrogenase I. J. Bacteriol. 173: 4851–4861
Miller JB & Amy NK (1983) Molybdenum cofactor in chlorate-resistant and nitrate reductase-deficient insertion mutants ofEscherichia coli. J. Bacteriol. 155: 793–801
Morpeth FF & Boxer DH (1985) Kinetic analysis of respiratory nitrate reductase fromEscherichia coli K-12. Biochemistry 24: 40–46
Motteram PAS, McCarthy JEG, Ferguson SJ, Jackson JB & Cole JA (1981) Energy conservation during the formate-dependent reduction of nitrite byEscherichia coli. FEMS Microbiol. Lett. 12: 317–320
Nagy PL, McCorkle GM & Zalkin H (1993)purU, a source of formate forpurT-dependent phosphoribosyl-N-formylglycinamide synthesis. J. Bacteriol. 175: 7066–7073
Navarro C, Wu L-F & Mandrand-Berthelot M-A (1993) Thenik operon ofEscherichia coli encodes a periplasmic binding-protein-dependent transport system for nickel. Mol. Microbiol. 9: 1181–1191
Newman BM & Cole JA (1978) The chromosomal location and pleiotropic effects of mutations in thenirA + gene ofEscherichia coli K12: the essential role ofnirA + in nitrite reduction and in other anaerobic redox reactions. J. Gen. Microbiol. 106: 1–12
Noji S, Nohno T, Saito T & Taniguchi S (1989) ThenarK gene product participates in nitrate transport induced inEscherichia coli nitrate-respiring cells. FEBS Lett. 252: 139–143
Ordal EJ & Halvorson HO (1939) A comparison of hydrogen production from sugars and formic acid by normal and variant strains ofEscherichia coli. J. Bacteriol. 38: 199–220
Page L, Griffiths L & Cole JA (1990) Different physiological roles for two independent pathways for nitrite reduction to ammonia by eneteric bacteria. Arch. Microbiol. 154: 249–354
Parkinson JS & Kofoid EC (1992) Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26: 71–112
Pascal M-C, Casse F, Chippaux M & Lepelletier M (1975) Genetic analysis of mutants ofEscherichia coli K12 andSalmonella typhimurium LT2 deficient in hydrogenase activity. Mol. Gen. Genet. 141: 173–179
Paveglio MT, Tang JS, Unger RE & Barrett EL (1988) Formatenitrate respiration inSalmonella typhimurium: studies of tworha-linkedfdn genes. J. Bacteriol. 170: 213–217
Pecher A, Zinoni F & Böck A (1985) The seleno-polypeptide of formic dehydrogenase (formate hydrogen-lyase linked) fromEscherichia coli: genetic analysis. Arch. Microbiol. 141: 359–363
Pecher A, Zinoni F, Jatsatienr C, Wirth R, Hennecke H & Böck A (1983) On the redox control of synthesis of anaerobically induced enzymes in enterobacteriaceae. Arch. Microbiol. 136: 131–136
Peck HD & Gest H (1957) Formic dehydrogenase and the hydrogenlyase enzyme complex in coli-aerogenes bacteria. J. Bacteriol. 73: 706–721
Pinsent J (1954) The need for selenite and molybdate in the formation of formic dehydrogenase by members of the coli-aerogenes group of bacteria. Biochem. J. 57: 10–16
Pinsky MJ & Stokes JL (1952) Requirements for formic hydrogenlyase adaptation in nonproliferating suspensions ofEschericia coli. J. Bacteriol. 64: 151–161
Plunkett G, Burland V, Daniels DL & Blattner FR (1993) Analysis of theEscherichia coli genome. III. DNA sequence of the region from 87.2 to 89.2 minutes. Nucl. Acids Res. 21: 3391–3398
Pommier J, Mandrand M-A, Holt SE, Boxer DH & Giordano G (1992) A second phenazine methosulphate-linked formate dehydrogenase isoenzyme inEscherichia coli. Biochim. Biophys. Acta 1107: 305–313
Przybyla AE, Menon NK, Robbins J, DerVartanian L & Peck HD (1991) Further characterisation of thehya andhyb operons ofEscherichia coli. In: Abstracts of 3rd International Conference on the Molecular Biology of Hydrogenases. Troia, Portugal
Przybyla AE, Robbins J, Menon N & Peck HD (1992) Structure-function relationships among nickel-containing hydrogenases. FEMS Microbiol. Rev. 88: 109–136
Rabin RS, Collins LA & Stewart V (1992)In vivo requirement of integration host factor fornar (nitrate reductase) operon expression inEscherichia coli K-12. Proc. Natl. Acad. Sci. USA 89: 8701–8705
Rabin RS & Stewart V (1992) Either of two functionally redundant sensor proteins, NarX and NarQ, is sufficient for nitrate regulation inEscherichia coli K-12. Proc. Natl. Acad. Sci. USA 89: 8419–8423
Rabin RS & Stewart V (1993) Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression inEscherichia coli K-12. J. Bacteriol. 175: 3259–3268
Radman M, Wagner RE, Glickman BW & Meselson M (1980) DNA methylation mismatch correction and genetic stability, In: Alecivic M (Ed) Progress in Environmental Mutagenesis (pp 121–130). Elsevier, Amsterdam
Rajagopalan KV & Johnson JL (1992) The pterin molybdenum cofactors. J. Biol. Chem. 267: 10199–10202
Rey L, Murillo J, Hernando Y, Hidalgo E, Cabrera E, Imperial J & Ruiz-Argüeso T (1993) Molecular analysis of a microaerobically induced operon required for hydrogenase synthesis inRhizobium leguminosarum bv.viciae. Mol. Microbiol. 8: 471–481
Rivers SL, McNairn E, Blasco F, Giordano G & Boxer DH (1993) Molecular genetic analysis of themoa operon ofEscherichia coli K-12 required for molybdenum cofactor biosynthesis. Mol. Microbiol. 8: 1071–1082
Rohde M, Furstenau V, Mayer F, Przybyla AE, Peck HD, LeGall J, Choi E-S & Menon NK (1989) Localisation of membrane-associated (NiFe) and (NiFeSe) hydrogenases ofDesulfovibrio vulgaris using immunoelectron microscopic procedures. Eur. J. Biochem. 180: 421–427
Rossmann R, Sauter M, Lottspeich F & Böck A (1994) Maturation of the large subunit (HycE) of hydrogenase 3 ofEscherichia coli requires nickel incorporation followed by C-terminal processing at Arg537. Eur. J. Biochem. (in press)
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
Ruiz-Herrera J & Alvarez A (1972) A physiological study of formate dehydrogenase, formate oxidase and hydrogenlyase fromEscherichia coli K-12. Antonic van Leeuwenhoek 38: 479–491
Ruiz-Herrera J & DeMoss JA (1969) Nitrate reductase complex ofEscherichia coli K-12: participation of specific formate dehydrogenase and cytochromeb 1 components in nitrate reduction. J. Bacteriol. 99: 720–729
Ruiz-Herrera J, Showe MK & DeMoss JA (1969) Nitrate reductase complex ofEscherichia coli K-12: isolation and characterisation of mutants unable to reduce nitrate. J. Bacteriol. 97: 1291–1297
Sankar P, Lee JH & Shanmugam KT (1985) Cloning of hydrogenase genes and fine structure analysis of an operon essential for hydrogen metabolism inEscherichia coli. J. Bacteriol. 162: 353–360
Sankar P, Lee JH & Shanmugam KT (1988) Gene-product relationships offhlA andfdv genes ofEscherichia coli. J. Bacteriol. 170: 5440–5445
Sankar P & Shanmugam KT (1988a) Biochemical and genetic analysis of hydrogen metabolism inEscherichia coli: thehydB gene. J. Bacteriol. 170: 5433–5439
Sankar P & Shanmugam KT (1988b) Hydrogen metabolism inEscherichia coli: biochemical and genetic evidence for ahydF gene. J. Bacteriol. 170: 5446–5451
Santini C-L, Iobbi-Nivol C, Romane C, Boxer DH & Giordano G (1992) Molybdoenzyme biosynthesis inEscherichia coli: in vitro activation of purified nitrate reductase from achlB mutant. J. Bacteriol. 174: 7934–7940
Sauter M, Böhm R & Böck A (1992) Mutational analysis of the operon (hyc) determining hydrogenase 3 formation inEscherichia coli. Mol. Microbiol. 6: 1523–1532
Sawers G (1985) Membrane-bound hydrogenase isoenzymes fromEscherichia coli. Ph.D. thesis, University of Dundee
Sawers G (1993) Specific transcriptional requirements for positive regulation of the anaerobically induciblepfl operon by ArcA and FNR. Mol. Microbiol. 10: 737–747
Sawers G & Böck A (1988) Anaerobic regulation of pyruvate formate-lyase fromEscherichia coli K-12. J. Bacteriol. 170: 5330–5336
Sawers G & Böck A (1989) Novel transcriptional control of the pyruvate formate-lyase gene: upstream regulatory sequences and multiple promoters regulate anaerobic expression. J. Bacteriol. 171: 2485–2498
Sawers G, Heider J, Zehelein E & Böck A (1991) Expression and operon structure of thesel genes ofEscherichia coli and identification of a third selenium-containing formate dehydrogenase isoenzyme. J. Bacteriol. 173: 4983–4993
Sawers G & Suppmann B (1992) Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins. J. Bacteriol. 174: 3474–3478
Sawers RG, Ballantine SP & Boxer DH (1985) Differential expression of hydrogenase isoenzymes inEscherichia coli K-12: evidence for a third isoenzyme. J. Bacteriol. 164: 1324–1331
Sawers RG & Boxer DH (1986) Purification and properties of membrane-bound hydrogenase isoenzyme 1 from anaerobically grownEscherichia coli K12. Eur. J. Biochem. 156: 265–275
Sawers RG, Jamieson DJ, Higins CF & Boxer DH (1986) Characterisation and physiological roles of membrane-bound hydrogenase isoenzymes fromEscherichia coli. J. Bacteriol. 168: 398–404
Schlensog V, Birkmann A & Böck A (1989) Mutations intrans which affect the anaerobic expression of a formate dehydrogenase (fdhF) structural gene. Arch. Microbiol. 152: 83–89
Schlensog V & Böck A (1990) Identification and sequence analysis of the gene encoding the transcriptional activator of the formate hydrogenlyase system ofEscherichia coli. Mol. Microbiol. 4: 1319–1327
Schlensog V & Böck A (1991) TheEscherichia coli fdv gene probably encodes MutS and is located at minute 58.8 adjacent to thehyc-hyp gene cluster. J. Bacteriol. 173: 7414–7415
Schlensog V, Lutz S & Böck A (1994) Purification and DNA-binding properties of FHLA, the transcriptional activator of the formate hydrogenlyase system fromE. coli. J. Biol. Chem. in press
Schlindwein C, Giordano G, Santini C-L & Mandrand-Berthelot M-A (1990) Identification and expression of theEscherichia coli fdhD andfdhE genes, which are involved in the formation of respiratory formate dehydrogenase. J. Bacteriol. 172: 6112–6121
Schlindwein C & Mandrand M-A (1991) Nucleotide sequence of thefdhE gene involved in respiratory formate dehydrogenase formation inEscherichia coli K-12. Gene 97: 147–148
Schröder I, Darie S & Gunsalus RP (1992) Activation of theEscherichia coli nitrate reductase (narGHJI) operon by NarL and FNR requires integration host factor. J. Biol. Chem. 268: 771–774
Scott RH & DeMoss JA (1976) Formation of the formate-nitrate electron transport pathway from inactive components inEscherichia coli. J. Bacteriol. 126: 478–486
See YP & Glick BR (1982) Analysis of the expression of cloned genes using anEscherichia coli cell-free system. Can. J. Biochem. 60: 1095–1100
Shanmugam KT, Stewart V, Gunsalus RP, Boxer DH, Cole JA, Chippaux M, DeMoss JA, Giordano G, Lin ECC & Rajagopalan KV (1992) Proposed nomenclature for the genes involved in molybdenum metabolism inEscherichia coli andSalmonella typhimurium. Mol. Microbiol. 6: 3452–3454
Shuber AP, Orr EC, Recny MA, Schendel PF, May HD, Schauer NL & Ferry JG (1986) Cloning, expression, and nucleotide sequence of the formate dehydrogenase genes fromMethanobacterium formicicum. J. Biol. Chem. 261: 12943–12947
Shum A & Murphy JC (1972) Effects of selenium compounds on formate metabolism and coincidence of selenium-75 incorporation and formic dehydrogenase activity in cell-free preparations ofEscherichia coli. J. Bacteriol. 110: 447–449
Spiro S & Guest JR (1990) FNR and its role in oxygen-regulated gene expression inEscherichia coli. FEMS Microbiol. Rev. 75: 399–428
Stadtman TC (1990) Selenium biochemistry. Annu. Rev. Biochem. 59: 111–127
Stadtman TC, Davis JN, Ching W-M, Zinoni F & Böck A (1991) Amino acid sequence analysis ofEscherichia coli formate dehydrogenase (FDH H ) confirms that TGA in the gene encodes selenocysteine in the gene product. BioFactors 3: 21–27
Stadtman TC, Davis JN, Zehelein E & Böck A (1989) Biochemical and genetic analysis ofSalmonella typhimurium andEscherichia coli mutants defective in specific incorporation of selenium into formate dehydrogenase and tRNAs. BioFactors 2: 35–44
Stephenson M & Stickland LH (1931) Hydrogenase: a bacterial enzyme activating molecular hydrogen. I. The properties of the enzyme. Biochem. J. 25: 205–214
Stephenson M & Stickland LH (1932) Hydrogenlyases. Bacterial enzymes liberating molecular hydrogen. Biochem. J. 26: 712–724
Stewart V (1988) Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol. Rev. 52: 190–232
Stewart V (1993) Nitrate regulation of anaerobic respiratory gene expression inEscherichia coli. Mol. Microbiol. 9: 425–434
Stewart V & Berg BL (1988) Influence ofnar (nitrate reductase) genes in nitrate inhibition of formate-hydrogen lyase and fumarate reductase gene expression inEscherichia coli K-12. J. Bacteriol. 170: 4437–4444
Stewart V, Lin JT & Berg BL (1991) Genetic evidence that genesfdhD andfdhE do not control synthesis of formate dehydrogenase-N inEscherichia coli K-12. J. Bacteriol. 173: 4417–4423
Stewart V & MacGregor CH (1982) Nitrate reductase inEscherichia coli K-12: involvement ofchlC, chlE andchlG loci. J. Bacteriol. 151: 788–799
Stoker K, Oltmann LF & Stouthamer AH (1988) Partial characterisation of an electrophoretically labile hydrogenase activity ofEscherichia coli K-12. J. Bacteriol. 170: 1220–1226
Stoker K, Oltmann LF & Stouthamer AH (1989a) Randomly inducedEscherichia coli K-12 Tn5 insertion mutants defective in hydrogenase activity. J. Bacteriol. 171: 831–836
Stoker K, Reijnders WNM, Oltmann LF & Stouthamer AH (1989b) Initial cloning and sequencing ofhydGH, an operon homologous tontrBC and regulating the labile hydrogenase activity inEscherichia coli K-12. J. Bacteriol. 171: 4448–4456
Suppmann B & Sawers G (1994) Isolation and characterisation of hypophsphite-resistant mutants ofEscherichia coli: identification of the FocA protein, encoded nby thepfl operon, as a putative formate transporter. Mol. Microbiol. 11: 965–982
Tomiyama M, Shiotani M, Sode K, Tamiya E & Karube I (1991) Nucleotide sequence analysis and expression control ofhydA inEscherichia coli. In: Abstracts of 3rd International Conference on the Molecular Biology of Hydrogenases. Troia, Portugal
Van der Zwaan JW, Albracht SPJ, Fontijn RD & Slater EC (1985) Monovalent nickel in hydrogenase fromChromatium vinosum: light sensitivity and evidence for direct interaction with hydrogen. FEBS Lett. 179: 271–277
Veres Z, Tsai L, Scholz TD, Politino M, Balaban RS & Stadtman TC (1992) Synthesis of 5-methylaminomethyl-2-selenouridine in tRNAs:31P NMR studies show how the labile selenium donor synthesised by theselD gene product contains selenium bonded to phosphorus. Proc. Natl. Acad. Sci. USA 89: 2975–2979
Vignais PM & Toussaint B (1994) Molecular biology of membrane-bound H2 uptake hydrogenases. Arch. Microbiol. 161: 1–10
Voordouw G (1992) Evolution of hydrogenase genes. Adv. Inorg. Chem. 38: 397–422
Wagner AFV, Frey M, Neugebauer FA, Schäfer W & Knappe J (1992) The free radical in pyruvate formate-lyase is located on glycine-734. Proc. Natl. Acad. Sci. USA 89: 996–1000
Waugh R & Boxer DH (1986) Pleiotropic hydrogenase mutants ofEscherichia coli K12: growth in the presence of nickel can restore hydrogenase activity. Biochimie 68: 157–166
Weiss H, Friedrich T, Hofhaus G & Preis D (1991) The respiratory chain NADH dehydrogenase (complex I) of mitochondria. Eur. J. Biochem. 197: 563–576
Wendt JC, Maupin JA & Shanmugam KT (1991) Physiological and genetic regulation of dihydrogen metabolism inEscherichia coli. In: Abstracts of the 3rd International Conference on the Molecular Biology of Hydrogenses. Troia, Portugal
Wimpenny JWT & Cole JA (1967) The regulation of metabolism in facultative bacteria. III. The effect of nitrate. Biochim. Biophys. Acta 148: 133–242
Wu L-F & Mandrand-Berthelot M-A (1986a) Molecular cloning of thefdhF gene ofEscherichia coli K-12. FEMS Microbiol. Lett. 34: 323–327
Wu L-F & Mandrand M-A (1993) Microbial hydrogenases: primary structure, classification, signatures and phylogeny. FEMS Microbiol. Rev. 104: 243–270
Wu L-F & Mandrand-Berthelot M-A (1986b) Genetic and physiological characterisation of newEscherichia coli mutants impaired in hydrogenase activity. Biochimie 68: 167–179
Wu L-F & Mandrand-Berthelot M-A (1987) Regulation of thefdhF gene encoding the selenopolypeptide for benzyl viologen-linked formate dehydrogenase inEscherichia coli. Mol. Gen. Genet. 209: 129–134
Wu L-F, Mandrand-Berthelot M-A, Waugh R, Edmonds CJ, Holt SE & Boxer DH (1989) Nickel deficiency gives rise to the defective hydrogenase phenotype ofhydC andfnr mutants inEscherichia coli. Mol. Microbiol. 3: 1709–1718
Wu L-F, Navarro C & Mandrand-Berthelot M-A (1991) ThehydC region contains a multi-cistronic operon (nik) involved in nickel transport inEscherichia coli. Gene 107: 37–42
Yamamoto I & Ishimoto M (1978) Hydrogen-dependent growth ofEscherichia coli in anaerobic respiration and the presence of hydrogenases with different functions. J. Biochem. (Tokyo) 84: 673–679
Yamamoto T, Tomiyama M, Mita H, Sode K & Karube I (1990) Identification of protcins encoded inEscherichia coli hydA, hydB and analysis of thehydA locus. FEMS Microbiol. Lett. 66: 187–192
Yerkes JH, Casson LP, Honkanen AK & Walker GC (1984) Anaerobiosis induces expression ofant, a newEscherichia coli locus with a role in anaerobic electron transport. J. Bacteriol. 158: 180–186
Zinoni F, Beier A, Pecher A, Wirth R & Böck A (1984) Regulation of the synthesis of hydrogenase (formate hydrogen-lyase linked) ofE. coli. Arch. Microbiol. 139: 299–304
Zinoni F, Birkmann A, Leinfelder W & Böck A (1987) Cotranslational insertion of selenocysteine into formate dehydrogenase fromEscherichia coli directed by a UGA codon. Proc. Natl. Acad. Sci. USA 84: 3156–3160
Zinoni F, Birkmann A, Stadtman TC & Böck A (1986) Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyaselinked) fromEscherichia coli. Proc. Natl. Acad. Sci. USA 83: 4650–4654
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Sawers, G. The hydrogenases and formate dehydrogenases ofEscherichia coli . Antonie van Leeuwenhoek 66, 57–88 (1994). https://doi.org/10.1007/BF00871633
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DOI: https://doi.org/10.1007/BF00871633