Abstract
This paper focuses on the group of metalloproteins/metalloenzymes in the acetyl-coenzyme A synthesis pathway of anaerobic microbes called Wood-Ljungdahl pathway, including formate dehydrogenase (FDH), corrinoid iron sulfur protein (CoFeSP), acetyl-CoA synthase (ACS) and CO dehydrogenase (CODH). FDH, a key metalloenzyme involved in the conversion of carbon dioxide to methyltetrahydrofolate, catalyzes the reversible oxidation of formate to carbon dioxide. CoFeSP, as a methyl group transformer, accepts the methyl group from CH3-H4 folate and then transfers it to ACS. CODH reversibly catalyzes the reduction of CO2 to CO and ACS functions for acetyl-coenzyme A synthesis through condensation of the methyl group, CO and coenzyme A, to finish the whole pathway. This paper introduces the structure, function and reaction mechanisms of these enzymes.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Berg J M, Tymoczko J L, Stryer L. Biochemistry. 5th ed. New York: W. H. Freeman and Co., 2002. 697–733
Ragsdale S W. Life with carbon monoxide. Crit Rev Biochem Mol, 2004, 39(3): 165–195
Ragsdale S W. Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann N Y Acad Sci, 2008, 1125: 129–136
Muller V. Energy conservation in acetogenic bacteria. Appl Environ Microbiol, 2003, 69(11): 6345–6353
Ferry J G. Formate dehydrogenase. FEMS Microbiol Rev, 1990, 7(3–4): 377–382
Popov V O, Lamzin V S. NAD(+)-dependent formate dehydrogenase. Biochem J, 1994, 301( Pt 3): 625–643
Jormakka M, Byrne B, Iwata S. Formate dehydrogenase. A versatile enzyme in changing environments. Curr Opin Struct Biol, 2003, 13(4): 418–423
Ljungdahl L G. Tungsten, a biologically active metal. Trends Biochem Sci, 1976, 1: 63–65
Andreesen J R. Role of selenium, molybdenum and tungsten in anaerobes. In: Gottschalk G, Pfennig N, Werner H. eds. Anaerobiosis and Anaerobic Infection. Stuttgart: Gustav Fischer Verlag, 1979. 4–32
Ljungdahl L G. The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu Rev Microbiol, 1986, 40: 415–450
Diekert G, Wohlfarth G. Metabolism of homoacetogens. Antonie van Leeuwenhoek, 1994, 66: 209–221
Ljungdahl L G. Formate dehydrogenases: Role of molybdenum, tungsten and selenium. In: Coughlan M P, ed. Molybdenum and Molybdenum-Containing Enzymes. New York: Pergamon Press Oxford, 1980. 463–486
Cardin C J, Mason J. Sulphate transport by rat ileum. Effect of molybdate and other anions. Biochim Biophys Acta, 1975, 394: 46–54
Tishkov V I, Popov V O. Protein engineering of formate dehydro-genase. Biomol Eng, 2006, 23: 89–110
Kletzin A, Adams M W W. Tungsten in biological systems. Fems Microbiol Rev, 1996, 18: 5–63
Jormakka M, Byrney B, Iwata S. Formate dehydrogenase. A versatile enzyme in changing environments. Curr Opin Struc Biol, 2003, 13: 418–423
Lamzin V S, Aleshin A E, Strokopytov B V, Yukhnevich M G, Popov V O, Harutyunyan E H, Wilson K S. Crystal structure of NAD-dependent formate dehydrogenase. Eur J Biochem, 1992, 206: 441–452
Romão M J, Archer M, Moura I, Moura J J G, LeGall J, Engh R, Schneider M, Hof P, Huber R. Crystal structure of the xanthine oxidase-related aldehyde oxido-reductase from D. gigas. Science, 1995, 270: 1170–1176
Chan M K, Mukund S, Kletzin A, Adams M W W, Rees D C. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science, 1995, 267: 1463–1469
Schindelin H, Kisker C, Hilton J, Rajagopalan K V, Rees D C. The overall fold of Rhodobacter sphaeroides DMSO reductase is similar to that of FDHH. Science, 1996, 272: 1615–1622
Huber R, Hof P, Duarte R O, Moura J J G, Moura I, Liu M Y, LeGall J, Hille R, Archer M, Romão M J. A structure-based catalytic mechanism for the xanthine oxidase family of molybdenum enzymes. Proc Natl Acad Sci USA, 1996, 93: 8846–8851
Boyington J C, Gladyshev V N, Khangulov S V, Stadtman T C, Sun P D. Crystal structure of formate dehydrogenase H: Catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science, 1997, 275: 1305–1308
Jormakka M, Tornroth S, Byrne B, Iwata S. Molecular basis of proton motive force generation: Structure of formate dehydrogenase-N. Science, 2002, 295: 1863–1868
Raaijmakers H, Macieira S, Dias J M, Teixeira S, Bursakov S, Huber R, Moura J J, Moura I, Romao M J. Gene sequence and the 1.8 A crystal structure of the tungsten-containing formate dehydrogenase from desulfovibrio gigas. Structure, 2002, 10: 1261–1272
Filippova E V, Polyakov K M, Tikhonova T V, Stekhanova T N, Boiko K M, Popov V O. Structure of a new crystal modification of the bacterial NAD-dependent formate dehydrogenase with a resolution of 2.1A. Crystallogr Rep, 2005, 50(5): 796–800
Filippova E V, Polyakov K M, Tikhonova T V, Stekhanova T N, Boiko K M, Sadykhov I G, Tishkov V I, Popov V O, Labru N. Crystal structures of complexes of NAD+-dependent formate dehydrogenase from methylotrophic bacterium Pseudomonas sp. 101 with formate. Crystallogr Rep, 2006, 51(4): 627–631
Böck A, Stadtman T C. Selenocysteine, a highly specific component of certain enzymes, is incorporated by a UGA-directed co-translational mechanism. Biofactors, 1988, 1(3): 245–250
Humphrey W, Dalke A, Schulten K. VMD-visual molecular dynamics. J Molec Graphics, 1996, 14: 33–38
Khangulov S V, Gladyshev V N, Dismukes G C, Stadtman T C. Selenium-containing formate dehydrogenase H from Escherichia coli: A molybdopterin enzyme that catalyzes formate oxidation without oxygen transfer. Biochemistry, 1998, 37: 3518–3528
Yamamoto I, Saiki T, Liu S M, Ljungdahl L G. Purification and properties of NADP-dependent formate dehydrogenase from Clostridium thermoaceticum, a tungsten-selenium-iron protein. J Biol Chem, 1983, 258(3): 1826–1832
Hu S I, Pezacka E, Wood H G. Acetate synthesis from carbon monoxide by Clostridium thermoaceticum. Purification of the corrinoid protein. J Biol Chem, 1984, 259: 8892–8897
Maupin F J, Ferry J G. Analysis of the CO dehydrogenase/acetylcoenzyme A synthase operon of Methanosarcina thermophila. J Bacteriol, 1996, 178: 340–346
Svetlitchnyi V, Dobbek H, Meyer-Klaucke W, Meins T, Thiele B, Romer P, Huber R, Meyer O. A functional Ni-Ni-[4Fe-4S] cluster in the monomeric acetyl-CoA synthase from Carboxydothermus hydrogenoformans. Proc Natl Acad Sci USA, 2004, 101: 446–451
Svetlitchnaia T, Svetlitchnyi V, Meyer O, Dobbek H. Structural insights into methyltransfer reactions of a corrinoid iron-sulfur protein involved in acetyl-CoA synthesis. Proc Natl Acad Sci USA, 2006, 103 (39): 14331–14336
Funk T, Gu W W, Friedrich S, Wang H X, Gencic S, Grahame D A, Cramer S P. Chemically distinct Ni sites in the A-cluster in subunit β of the acetyl-CoA decarbonylase/synthase complex from Methanosarcina thermophila: Ni L-edge absorption and X-ray magnetic circular dichroism analyses. J Am Chem Soc, 2004, 126 (1): 88–95
Dobbek H, Svetlitchnyi V, Gremer L, Huber R, Meyer O. Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science, 2001, 293: 1281–1285
Drennan C L, Heo J, Sintchak M D, Schreiter E, Ludden P W. Redox-dependent activation of CO dehydrogenase from Rhodospirillum rubrum. Proc Natl Acad Sci USA, 2001, 98: 11973–11978
Doukov T I, Iverson T M, Seravalli J, Ragsdale S W, Drennan C L. A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Science, 2002, 298: 567–572
Darnault C, Volbeda A, Kim E J, Legrand P, Vernede X, Lindahl P A, Fontecilla-Camps J C. Ni-Zn-[Fe-4-S-4] and Ni-Ni-[Fe-4.S-4] clusters in closed and open subunits of acetyl-CoA synthase/carbon monoxide dehydrogenase. Nat Struct Mol Biol, 2003, 10(4): 271–279
Svetlitchnyi V, Dobbek H, Meyer-Klaucke W, Meins T, Thiele B, Romer P, Huber R, Meyer O. Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase. Proc Natl Acad Sci USA, 2004, 101: 446–451
Jeoung J H, Dobbek H. Carbon dioxide activation at the Ni, Fe-cluster of anaerobic carbon monoxide dehydrogenase. Science, 2007, 318: 1461–1464
Lindahl P A. The Ni-containing carbon monoxide dehydrogenase family: Light at the end of the tunnel. Biochemistry, 2002, 41: 2097–2105
Kim E J, Feng J, Bramlett M R, Lindahl P A. Carbon monoxide dehydrogenase from Rhodospirillum rubrum: Effect of redox potential on catalysis. Biochemistry, 2004, 43: 5728–5734
Hu Z, Spangler N J, Anderson M E, Xia J, Ludden P W, Lindahl P A, Munck E. Nature of the C-cluster in Ni-containing carbon monoxide dehydrogenases. J Am Chem Soc, 1996, 118: 830–845
DeRose V J, Telser J, Anderson M E, Lindahl P A, Hoffman B M. A multinuclear ENDOR study of the C-cluster in CO dehydrogenase from Clostridium thermoaceticum: Evidence for HxO and histidine coordination to the [Fe4S4] center. J Am Chem Soc, 1998, 120: 8767–8776
Fraser D M, Lindahl P A. Evidence for a proposed intermediate redox state in the CO/CO2 active site of acetyl-CoA synthase (carbon monoxide dehydrogenase) from Clostridium thermoaceticum. Biochemistry, 1999, 38: 15706–15711
Loke H K, Tan X S, Lindahl P A. Genetic construction of truncated and chimeric metalloproteins derived from the alpha subunit of acetyl-CoA synthase from Clostridium thermoaceticum. J Am Chem Soc, 2002, 124(29): 8667–8672
Tan X S, Bramlett M R, Lindahl P A. Effect of Zn on acetyl coenzyme a synthase: Evidence for a conformational change in the a subunit during catalysis. J Am Chem Soc, 2004, 126(19): 5954–5955
Bramlett M R, Tan X S, Lindahl P A. Inactivation of acetyl-CoA synthase/carbon monoxide dehydrogenase by copper. J Am Chem Soc, 2003, 125(31): 9316–9317
Tan X S, Loke H K, Fitch S, Lindahl P A. The tunnel of the acetyl-CoA synthase/carbon monoxide dehydrogenase regulates delivery of CO to the active site. J Am Chem Soc, 2005, 127(16): 5833–5839
Tan X S, Volbeda A, Fontecilla-Camps J C, Lindahl P A. Function of the tunnel in acetyl-coenzyme A synthase/carbon monoxide dehydrogenase. J Biol Inorg Chem, 2006, 11(3): 371–378
Tan X S, Kagiampakis I, Surovtsev I V, Demeler B, Lindahl P A. Nickel-dependent oligomerization of the alpha subunit of acetyl-coenzyme a synthase/carbon monoxide dehydrogenase. Biochemistry, 2007, 46: 11606–11613
Tan X S, Surovtsev I V, Lindahl P A. Kinetics of CO insertion and acetyl-group transfer steps, and a model of the acetyl-coenzyme A synthase catalytic mechanism. J Am Chem Soc, 2006, 128(37): 12331–12338
Tan X S, Christopher S, Lindahl P A. Stopped-flow kinetic of methyl group transfer between corrinoid-iron-sulfur protein and acetyl-coenzyme A synthase from Clostridium thermoaceticum. J Am Chem Soc, 2002, 124(22): 6277–6284
Tan X S, Sewell C, Yang Q W, Lindahl P A. Reduction and methyl transfer kinetics of alpha subunit from acetyl-coenzyme A synthase. J Am Chem Soc, 2003, 125(2): 318–319
Seravalli J, Ragsdale S W. Pulse-chase studies of the synthesis of acetyl-CoA by carbon monoxide dehydrogenase/acetyl-CoA synthase. Evidence for a random mechanism of methyl and carbonyl addition. J Biol Chem, 2008, 283(13): 8384–8394
Grahame D A. Acetate C-C bond formation and decomposition n the anaerobic world: The structure of a central enzyme and its key active-site metal cluster. Trends Biochem Sci, 2003, 28(5): 221–224
Grahame D A. Catalysis of acetyl-CoA cleavage and tetrahydrosarcinapterin methylation by a cabon-monoxide dehydrogenase-corrinoid enzyme complex. J Biol Chem, 1991, 266: 22227–22233
Grahame D A, DeMoll E. Partial reactions catalyzed by protein components of the acetyl-CoA decarbonylase synthase enzyme complex from Methanosarcina barkeri. J Biol Chem, 1996, 271(14): 8352–8358
Bhaskar B, DeMoll E, Grahame D A. Redox-dependent acetyl transfer partial reaction of the acetyl-CoA decarbonylase/synthase complex: Kinetics and mechanism. Biochemistry, 1998, 37: 14491–14499
Kocsis E, Kessel M, DeMoll E, Grahame D A. Structure of the Ni/Fe-S protein subcomponent of the acetyl-CoA decarbonylase/synthase complex from Methanosarcina thermophila at 26-angstrom resolution. J Struct Biol, 1999, 128: 165–174
Balbo P, Oliveira M. Crystallization and preliminary X-ray data of the α2ε2 subcomponent of the acetyl-CoA decarbonylase/synthase multienzyme complex from Methanosarcina thermophila. Acta Crystallogr D Biol Crystallogr, 2003, 59: 721–723
Sebaihia M, Wren B W, Mullany P, Fairweather N F, Minton N, Stabler R, Thomson N R, Roberts A P, Cerdeno-Tarraga A M, Wang H, Holden M T, Wright A, Churcher C, Quail M A, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile mosaic genome. Nat Genet, 2006, 38 (7): 779–786
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by the National Natural Science Foundation of China (Grant No. 20771029), Shanghai Pujiang Talent Project (Grant No. 08PJ14017) and Shanghai Leading Academic Discipline Project (Grant No. B108)
Rights and permissions
About this article
Cite this article
Zhu, X., Tan, X. Metalloproteins/metalloenzymes for the synthesis of acetyl-CoA in the Wood-Ljungdahl pathway. Sci. China Ser. B-Chem. 52, 2071–2082 (2009). https://doi.org/10.1007/s11426-009-0082-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11426-009-0082-3