Carbon monoxide dehydrogenase explained

In enzymology, carbon monoxide dehydrogenase (CODH) is an enzyme that catalyzes the chemical reaction

CO + H2O + A

\rightleftharpoons

CO2 + AH2

The chemical process catalyzed by carbon monoxide dehydrogenase is similar to the water-gas shift reaction.

The 3 substrates of this enzyme are CO, H2O, and A, whereas its two products are CO2 and AH2.

A variety of electron donors/receivers (Shown as "A" and "AH2" in the reaction equation above) are observed in micro-organisms which utilize CODH. Several examples of electron transfer cofactors have been proposed, including Ferredoxin, NADP+/NADPH and flavoprotein complexes like flavin adenine dinucleotide (FAD) as well as hydrogenases.[1] [2] [3] [4] CODHs support the metabolisms of diverse prokaryotes, including methanogens, aerobic carboxidotrophs, acetogens, sulfate-reducers, and hydrogenogenic bacteria. The bidirectional reaction catalyzed by CODH plays a role in the carbon cycle allowing organisms to both make use of CO as a source of energy and utilize CO2 as a source of carbon. CODH can form a monofunctional enzyme, as is the case in Rhodospirillum rubrum, or can form a cluster with acetyl-CoA synthase as has been shown in M. thermoacetica. When acting in concert, either as structurally independent enzymes or in a bifunctional CODH/ACS unit, the two catalytic sites are key to carbon fixation in the reductive acetyl-CoA pathway. Microbial organisms (Both aerobic and anaerobic) encode and synthesize CODH for the purpose of carbon fixation (CO oxidation and CO2 reduction). Depending on attached accessory proteins (A,B,C,D-Clusters), serve a variety of catalytic functions, including reduction of [4Fe-4S] clusters and insertion of nickel.[5]

This enzyme belongs to the family of oxidoreductases, specifically those acting on the aldehyde or oxo group of donor with other acceptors. The systematic name of this enzyme class is carbon-monoxide:acceptor oxidoreductase. Other names in common use include anaerobic carbon monoxide dehydrogenase, carbon monoxide oxygenase, carbon-monoxide dehydrogenase, and carbon-monoxide:(acceptor) oxidoreductase.

Diversity

CODH are a rather diverse group of enzymes, containing two unrelated types of CODH. A copper-molybdenum flavoenzymes is found in some aerobic carboxydotrophic bacteria. Anaerobic bacteria utilize nickel-iron based CODHs.[6] [7] [8] Both classes of CODH catalyze the conversion of carbon monoxide (CO) to carbon dioxide (CO2). Only the Ni containing CODH is able to also catalyze the back reaction. CODHs exist in both monofunctional and bifunctional forms. An example for the latter case, Ni,Fe-CODHs form a bifunctional cluster with acetyl-CoA synthase, as has been well characterized in the anaerobic bacteria Moorella thermoacetica,[9] [10] Clostridium autoethanogenum [11] and Carboxydothermus hydrogenoformans [12] . While the ACS subunits of the complex of C. autoethanogenum show a rather extended arrangement those of the M. thermoacetica and C. hydrogenoformans complex are closer to the CODH subunits forming a tight tunnel network connecting cluster C and cluster A.

Ni,Fe-CODH

Nickel containing CODH (Ni,Fe-CODH) can be further divided into structural clades, dependent on their phylogenetic relationship[13]

Structure

Ni,Fe-CODH

Homodimeric Ni,Fe-CODHs contain five-metal clusters.[14] They exist either in a homodimeric form (also called monofunctional) or in a bifunctional α2β2-tetrameric complex with acetyl-CoA synthase (ACS).

Monofunctional

The best studied monofunctional CODHs are those of Desulfovibrio vulgaris, Rhodospirillum rubrum [15] [16] and Carboxydothermus hydrogenoformans. [17] [18] They are homodimers of around 130 kDa sharing a central [4Fe4S]-cluster at the surface of the protein - cluster D. The electrons are probably transferred to another [4Fe4S]-cluster (cluster B) located 10 A inside the protein and from there to the active site - cluster C, being an [Ni4Fe4S]-cluster.

Bifunctional

The CODH/ACS complex is an α2β2 tetrameric enzyme. The structures of CODH/ACS complexes of the anaerobic bacteria Moorella thermoacetica, Clostridium autoethanogenum and Carboxydothermus hydrogenoformans have been solved. The two CODH subunits form the central core of the enzyme to which an ACS subunit is attached at each side. Each α unit contains a single metal cluster. Together, the two β units contains five clusters of three types. CODH catalytic activity occurs at the Ni-[3Fe-4S] C-clusters while the interior [4Fe-4S] B and D clusters transfer electrons away from the C-cluster to external electron carriers such as ferredoxin. The ACS activity occurs in A-cluster located in the outer two α units.

All CODH/ACS complexes have a gas tunnel connecting the multiple active sites, while the tunnel system in the C. autoethanogenum enzyme is comparatively open and those of M. thermoacetica and C. hydrogenoformans rather tight. For the Moorella enzyme the rate of acetyl-CoA synthase activity from CO2 is not affected by the addition of hemoglobin, which would compete for CO in bulk solution,[19] and isotopic labeling studies show that carbon monoxide derived from the C-cluster is preferentially used at the A-cluster over unlabeled CO in solution.[20] Protein engineering of the CODH/ACS in M.thermoacetica revealed that mutating residues, so as to functionally block the tunnel, stopped acetyl-CoA synthesis when only CO2 was present.[21] The discovery of a functional CO tunnel places CODH on a growing list of enzymes that independently evolved this strategy to transfer reactive intermediates from one active site to another.[22]

Reaction mechanisms

Ni,Fe-CODH

The CODH catalytic site, referred to as the C-cluster, is a [3Fe-4S] cluster bonded to a Ni-Fe moiety. Two basic amino acids (Lys587 and His 113 in M.thermoacetica) reside in proximity to the C-cluster and facilitate acid-base chemistry required for enzyme activity.[23] Furthermore, other residues (i.e. an isoleucine apical to the Ni atom) fine-tune the binding and conversion of CO.[24] Based on IR spectra suggesting the presence of an Ni-CO complex, the proposed first step in the oxidative catalysis of CO to CO2 involves the binding of CO to Ni2+ and corresponding complexing of Fe2+ to a water molecule.[25]

It has been proposed that CO binds to square-planar nickel where it converts to a carboxy bridge between the Ni and Fe atom.[7] [26] A decarboxylation leads to the release of CO2 and the reduction of the cluster.

The electrons in the reduced C-cluster are transferred to nearby B and D [4Fe-4S] clusters, returning the Ni-[3Fe-4S] C-cluster to an oxidized state and reducing the single electron carrier ferredoxin.[27] [28]

Given CODH's role in CO2 fixation, the reductive mechanism is sometimes inferred as the “direct reverse” of the oxidative mechanism by the ”principle of microreversibility.”[29]

Environmental relevance

Carbon monoxide dehydrogenase regulates atmospheric CO and CO2 levels. Anaerobic micro-organisms like Acetogens undergo the Wood-Ljungdahl Pathway, relying on CODH to produce CO by reduction of CO2 needed for the synthesis of Acetyl-CoA from a methyl, coenzyme a (CoA) and corrinoid iron-sulfur protein.[29] Other types show CODH being utilized to generate a proton motive force for the purposes of energy generation. CODH is used for the CO oxidation, producing two protons which are subsequently reduced to form dihydrogen (H2.[30]

Further reading

Notes and References

  1. Buckel W, Thauer RK . Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD+ (Rnf) as Electron Acceptors: A Historical Review . Frontiers in Microbiology . 9 . 401 . 2018 . 29593673 . 5861303 . 10.3389/fmicb.2018.00401 . free .
  2. Kracke F, Virdis B, Bernhardt PV, Rabaey K, Krömer JO . Redox dependent metabolic shift in Clostridium autoethanogenum by extracellular electron supply . Biotechnology for Biofuels . 9 . 1 . 249 . December 2016 . 27882076 . 5112729 . 10.1186/s13068-016-0663-2 . free .
  3. van den Berg WA, Hagen WR, van Dongen WM . The hybrid-cluster protein ('prismane protein') from Escherichia coli. Characterization of the hybrid-cluster protein, redox properties of the [2Fe-2S] and [4Fe-2S-2O] clusters and identification of an associated NADH oxidoreductase containing FAD and [2Fe-2S] . European Journal of Biochemistry . 267 . 3 . 666–676 . February 2000 . 10651802 . 10.1046/j.1432-1327.2000.01032.x . free .
  4. Inoue M, Omae K, Nakamoto I, Kamikawa R, Yoshida T, Sako Y . Biome-specific distribution of Ni-containing carbon monoxide dehydrogenases . Extremophiles . 26 . 1 . 9 . January 2022 . 35059858 . 8776680 . 10.1007/s00792-022-01259-y .
  5. Hadj-Saïd J, Pandelia ME, Léger C, Fourmond V, Dementin S . The Carbon Monoxide Dehydrogenase from Desulfovibrio vulgaris . Biochimica et Biophysica Acta (BBA) - Bioenergetics . 1847 . 12 . 1574–1583 . December 2015 . 26255854 . 10.1016/j.bbabio.2015.08.002 . free .
  6. Book: Jeoung JH, Fesseler J, Goetzl S, Dobbek H . Kroneck PM, Torres ME . The Metal-Driven Biogeochemistry of Gaseous Compounds in the Environment . Metal Ions in Life Sciences . 14 . 2014 . Springer . Chapter 3. Carbon Monoxide. Toxic Gas and Fuel for Anaerobes and Aerobes: Carbon Monoxide Dehydrogenases . 37–69 . 10.1007/978-94-017-9269-1_3 . 25416390 .
  7. Dobbek H, Svetlitchnyi V, Gremer L, Huber R, Meyer O . Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster . Science . 293 . 5533 . 1281–1285 . August 2001 . 11509720 . 10.1126/science.1061500 . 21633407 . 2001Sci...293.1281D .
  8. Book: Ragsdale S . Metal-Carbon Bonds in Enzymes and Cofactors . . September 2010 . 10.1039/9781847559333 . Royal Society of Chemistry . 978-1-84755-915-9 . Metal Ions in Life Sciences . . . . . . Sigel H, Sigel A .
  9. Doukov TI, Blasiak LC, Seravalli J, Ragsdale SW, Drennan CL . Xenon in and at the end of the tunnel of bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase . Biochemistry . 47 . 11 . 3474–3483 . March 2008 . 18293927 . 3040099 . 10.1021/bi702386t .
  10. Tan X, Volbeda A, Fontecilla-Camps JC, Lindahl PA . Function of the tunnel in acetylcoenzyme A synthase/carbon monoxide dehydrogenase . Journal of Biological Inorganic Chemistry . 11 . 3 . 371–378 . April 2006 . 16502006 . 10.1007/s00775-006-0086-9 . 25285535 .
  11. Lemaire ON, Wagner T . Gas channel rerouting in a primordial enzyme: Structural insights of the carbon-monoxide dehydrogenase/acetyl-CoA synthase complex from the acetogen Clostridium autoethanogenum . Biochimica et Biophysica Acta (BBA) - Bioenergetics. 1862 . 1 . 148330 . January 2021 . 33080205 . 10.1016/j.bbabio.2020.148330 . 224825917 . free . 21.11116/0000-0007-F1AD-6 . free .
  12. Ruickoldt J, Basak Y, Domnik L, Jeoung JH, Dobbek H . 2022-10-21 . On the Kinetics of CO 2 Reduction by Ni, Fe-CO Dehydrogenases . ACS Catalysis . en . 12 . 20 . 13131–13142 . 10.1021/acscatal.2c02221 . 252880285 . 2155-5435. free .
  13. Inoue M, Nakamoto I, Omae K, Oguro T, Ogata H, Yoshida T, Sako Y . Structural and Phylogenetic Diversity of Anaerobic Carbon-Monoxide Dehydrogenases . Frontiers in Microbiology . 9 . 3353 . 2019-01-17 . 30705673 . 6344411 . 10.3389/fmicb.2018.03353 . free .
  14. Wittenborn EC, Merrouch M, Ueda C, Fradale L, Léger C, Fourmond V, Pandelia ME, Dementin S, Drennan CL . 6 . Redox-dependent rearrangements of the NiFeS cluster of carbon monoxide dehydrogenase . Clardy J, Cole PA, Clardy J, Rees DC. eLife . 7 . e39451 . October 2018 . 30277213 . 6168284 . 10.7554/eLife.39451 . free .
  15. Ensign SA, Bonam D, Ludden PW . Nickel is required for the transfer of electrons from carbon monoxide to the iron-sulfur center(s) of carbon monoxide dehydrogenase from Rhodospirillum rubrum . Biochemistry . 28 . 12 . 4968–4973 . June 1989 . 2504284 . 10.1021/bi00438a010 .
  16. Drennan CL, Heo J, Sintchak MD, Schreiter E, Ludden PW . Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase . Proceedings of the National Academy of Sciences of the United States of America . 98 . 21 . 11973–11978 . October 2001 . 11593006 . 59822 . 10.1073/pnas.211429998 . 2001PNAS...9811973D . free .
  17. Jeoung JH, Dobbek H . Structural basis of cyanide inhibition of Ni, Fe-containing carbon monoxide dehydrogenase . Journal of the American Chemical Society . 131 . 29 . 9922–9923 . July 2009 . 19583208 . 10.1021/ja9046476 .
  18. Jeoung JH, Dobbek H . Carbon dioxide activation at the Ni,Fe-cluster of anaerobic carbon monoxide dehydrogenase . Science . 318 . 5855 . 1461–1464 . November 2007 . 18048691 . 10.1126/science.1148481 . 2007Sci...318.1461J . 41063549 .
  19. Doukov TI, Iverson TM, Seravalli J, Ragsdale SW, Drennan CL . A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase . Science . 298 . 5593 . 567–572 . October 2002 . 12386327 . 10.1126/science.1075843 . 39880131 . 2002Sci...298..567D .
  20. Seravalli J, Ragsdale SW . Channeling of carbon monoxide during anaerobic carbon dioxide fixation . Biochemistry . 39 . 6 . 1274–1277 . February 2000 . 10684606 . 10.1021/bi991812e .
  21. Tan X, Loke HK, Fitch S, Lindahl PA . The tunnel of acetyl-coenzyme a synthase/carbon monoxide dehydrogenase regulates delivery of CO to the active site . Journal of the American Chemical Society . 127 . 16 . 5833–5839 . April 2005 . 15839681 . 10.1021/ja043701v .
  22. Weeks A, Lund L, Raushel FM . Tunneling of intermediates in enzyme-catalyzed reactions . Current Opinion in Chemical Biology . 10 . 5 . 465–472 . October 2006 . 16931112 . 10.1016/j.cbpa.2006.08.008 .
  23. Ragsdale SW . Metals and their scaffolds to promote difficult enzymatic reactions . Chemical Reviews . 106 . 8 . 3317–3337 . August 2006 . 16895330 . 10.1021/cr0503153 .
  24. Basak Y, Jeoung JH, Domnik L, Ruickoldt J, Dobbek H . 2022-10-21 . Substrate Activation at the Ni,Fe Cluster of CO Dehydrogenases: The Influence of the Protein Matrix . ACS Catalysis . en . 12 . 20 . 12711–12719 . 10.1021/acscatal.2c02922 . 252788375 . 2155-5435. free .
  25. Chen J, Huang S, Seravalli J, Gutzman H, Swartz DJ, Ragsdale SW, Bagley KA . Infrared studies of carbon monoxide binding to carbon monoxide dehydrogenase/acetyl-CoA synthase from Moorella thermoacetica . Biochemistry . 42 . 50 . 14822–14830 . December 2003 . 14674756 . 10.1021/bi0349470 .
  26. Ha SW, Korbas M, Klepsch M, Meyer-Klaucke W, Meyer O, Svetlitchnyi V . Interaction of potassium cyanide with the [Ni-4Fe-5S] active site cluster of CO dehydrogenase from Carboxydothermus hydrogenoformans . The Journal of Biological Chemistry . 282 . 14 . 10639–10646 . April 2007 . 17277357 . 10.1074/jbc.M610641200 . free .
  27. Book: Wang VC, Ragsdale SW, Armstrong FA . Investigations of the Efficient Electrocatalytic Interconversions of Carbon Dioxide and Carbon Monoxide by Nickel-Containing Carbon Monoxide Dehydrogenases . The Metal-Driven Biogeochemistry of Gaseous Compounds in the Environment . 14 . 71–97 . 2014 . 25416391 . 4261625 . 10.1007/978-94-017-9269-1_4 . Springer . Metal Ions in Life Sciences . 978-94-017-9268-4 . Martha E. Sosa Torres . Peter M.H. Kroneck .
  28. Ragsdale SW . Nickel and the carbon cycle . Journal of Inorganic Biochemistry . 101 . 11–12 . 1657–1666 . November 2007 . 17716738 . 2100024 . 10.1016/j.jinorgbio.2007.07.014 .
  29. Ragsdale SW, Pierce E . Acetogenesis and the Wood-Ljungdahl pathway of CO(2) fixation . Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics . 1784 . 12 . 1873–1898 . December 2008 . 18801467 . 2646786 . 10.1016/j.bbapap.2008.08.012 .
  30. Ensign SA, Ludden PW . Characterization of the CO oxidation/H2 evolution system of Rhodospirillum rubrum. Role of a 22-kDa iron-sulfur protein in mediating electron transfer between carbon monoxide dehydrogenase and hydrogenase . The Journal of Biological Chemistry . 266 . 27 . 18395–18403 . September 1991 . 1917963 . 10.1016/S0021-9258(18)55283-2 . free .

This article is licensed under the GNU Free Documentation License. It uses material from the Wikipedia article "Carbon monoxide dehydrogenase".

Except where otherwise indicated, Everything.Explained.Today is © Copyright 2009-2024, A B Cryer, All Rights Reserved. Cookie policy.