Evidence that ferredoxin interfaces with an internal redox shuttle in acetyl-CoA synthase during reductive activation and catalysis

Biochemistry

Volumn 50, Issue 2, 2011, Pages 276-286

  Bender, Güneş ^a   Ragsdale, Stephen W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL-COA; BIFUNCTIONAL; CATALYTIC CYCLES; ELECTRON ACCEPTOR; ELECTRON SHUTTLE; EPR SPECTRA; EXCHANGE REACTION; OXIDATION STATE; PARTIAL REACTIONS; REDOX MEDIATORS; REDOX SHUTTLE; REDOX-ACTIVE; REDUCTANTS; REDUCTION POTENTIAL; REDUCTIVE ACTIVATION; SYNTHASES;

CHEMICAL ACTIVATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRONS; SYNTHESIS (CHEMICAL);

REDOX REACTIONS;

ACETYL COENZYME A; CARBON MONOXIDE DEHYDROGENASE; FERREDOXIN; FERREDOXIN II; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; ELECTROCHEMICAL ANALYSIS; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; LIPID OXIDATION; MOORELLA THERMOACETICA; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; ULTRAVIOLET SPECTROSCOPY;

ACETYLATION; ALDEHYDE OXIDOREDUCTASES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROCHEMICAL TECHNIQUES; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME ACTIVATION; FERREDOXINS; METHYLATION; MOORELLA; MULTIENZYME COMPLEXES; OXIDATION-REDUCTION; PROTEIN SUBUNITS; SPECTROPHOTOMETRY, ULTRAVIOLET;

MOORELLA THERMOACETICA;

EID: 78651376724     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101511r     Document Type: Article

References (61)

1. Ragsdale, S. W. and Pierce, E. (2008) Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation Biochim. Biophys. Acta 1784, 1873-1898
2. Drake, H. L., Daniel, S. L., Kusel, K., Matthies, C., Kuhner, C., and Braus-Stromeyer, S. (1997) Acetogenic bacteria: what are the in situ consequences of their diverse metabolic versatilities? BioFactors 6, 13-24
3. Seravalli, J. and Ragsdale, S. W. (2008) 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. 283, 8384-8394
4. Loke, H. K., Tan, X. S., and Lindahl, P. A. (2002) Genetic construction of truncated and chimeric metalloproteins derived from the alpha subunit of acetyl-CoA synthase from Clostridium thermoaceticum J. Am. Chem. Soc. 124, 8667-8672
5. Gorst, C. M. and Ragsdale, S. W. (1991) Characterization of the NiFeCO complex of carbon-monoxide dehydrogenase as a catalytically competent intermediate in the pathway of acetyl-coenzyme-A synthesis J. Biol. Chem. 266, 20687-20693
6. Bramlett, M. R., Stubna, A., Tan, X. S., Surovtsev, I. V., Munck, E., and Lindahl, P. A. (2006) Mossbauer and EPR study of recombinant acetyl-CoA synthase from Moorella thermoacetica Biochemistry 45, 8674-8685
7. Maynard, E. L., Tan, X., and Lindahl, P. A. (2004) Autocatalytic activation of acetyl-CoA synthase J. Biol. Inorg. Chem. 9, 316-322
8. Tan, X. S., Sewell, C., Yang, Q. W., and Lindahl, P. A. (2003) Reduction and methyl transfer kinetics of the alpha subunit from acetyl coenzyme A synthase J. Am. Chem. Soc. 125, 318-319
9. 4](1+) Ni-p(1+)} A-cluster in isolated alpha subunits of acetyl-coenzyme a synthase/carbon monoxide dehydrogenase J. Am. Chem. Soc. 130, 6712-6713
10. Tan, X. S., Surovtsev, I. V., and Lindahl, P. A. (2006) Kinetics of CO insertion and acetyl group transfer steps, and a model of the acetyl-CoA synthase catalytic mechanism J. Am. Chem. Soc. 128, 12331-12338
11. Tan, X. S., Sewell, C., and Lindahl, P. A. (2002) Stopped-flow kinetics of methyl group transfer between the corrinoid-iron-sulfur protein and acetyl-coenzyme A synthase form Clostridium thermoaceticum J. Am. Chem. Soc. 124, 6277-6284
12. Barondeau, D. P. and Lindahl, P. A. (1997) Methylation of carbon monoxide dehydrogenase from Clostridium thermoaceticum and mechanism of acetyl coenzyme A synthesis J. Am. Chem. Soc. 119, 3959-3970
13. Seravalli, J., Kumar, M., and Ragsdale, S. W. (2002) Rapid kinetic studies of acetyl-CoA synthesis: evidence supporting the catalytic intermediacy of a paramagnetic NiFeC species in the autotrophic Wood-Ljungdahl pathway Biochemistry 41, 1807-1819
14. Lindahl, P. A. (2004) Acetyl-coenzyme A synthase: the case for a Ni-p(0)-based mechanism of catalysis J. Biol. Inorg. Chem. 9, 516-524
15. Ragsdale, S. W. (2007) Nickel and the carbon cycle J. Inorg. Biochem. 101, 1657-1666
16. Ragsdale, S. W., Ljungdahl, L. G., and Dervartanian, D. V. (1982) Electron-paramagnetic-res evidence for nickel-substrate interaction in carbon-monoxide dehydrogenase from Clostridium thermoaceticum Biochem. Biophys. Res. Commun. 108, 658-663
17. Fan, C. L., Gorst, C. M., Ragsdale, S. W., and Hoffman, B. M. (1991) Characterization of the Ni-Fe-C complex formed by reaction of carbon-monoxide with the carbon-monoxide dehydrogenase from Clostridium thermoaceticum by Q-band ENDOR Biochemistry 30, 431-435
18. Doukov, T. I., Iverson, T. M., Seravalli, J., Ragsdale, S. W., and Drennan, C. L. (2002) A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase Science 298, 567-572
19. Seravalli, J., Xiao, Y., Gu, W., Cramer, S. P., Antholine, W. E., Krymov, V., Gerfen, G. J., and Ragsdale, S. W. (2004) Evidence that NiNi acetyl-CoA synthase is active and that the CuNi enzyme is not Biochemistry 43, 3944-3955
20. Darnault, C., Volbeda, A., Kim, E. J., Legrand, P., Vernede, X., Lindahl, P. A., and Fontecilla-Camps, J. C. (2003) Ni-Zn-[Fe(4)-S(4)] and Ni-Ni-[Fe(4)-S(4)] clusters in closed and open alpha subunits of acetyl-CoA synthase/carbon monoxide dehydrogenase Nat. Struct. Biol. 10, 271-279
21. Drennan, C. L., Doukov, T. I., and Ragsdale, S. W. (2004) The metalloclusters of carbon monoxide dehydrogenase/acetyl-CoA synthase: a story in pictures J. Biol. Inorg. Chem. 9, 511-515
22. George, S. J., Seravalli, J., and Ragsdale, S. W. (2005) EPR and infrared spectroscopic evidence that a kinetically competent paramagnetic intermediate is formed when acetyl-coenzyme A synthase reacts with CO J. Am. Chem. So.c 127, 13500-13501
23. Bender, G., Stich, T. A., Yan, L., Britt, R. D., Cramer, S. P., and Ragsdale, S. W. (2010) Probing the catalytic mechanism of acetyl-CoA synthase by infrared and EPR characterization of the photolyzed Ni(I)-CO intermediate Biochemistry 49, 7516-7523
24. Menon, S. and Ragsdale, S. W. (1998) Role of the [4Fe-4S] cluster in reductive activation of the cobalt center of the corrinoid iron-sulfur protein from Clostridium thermoaceticum during acetyl-CoA synthesis Biochemistry 37, 5689-5698
25. Menon, S. and Ragsdale, S. W. (1999) The role of an iron-sulfur cluster in an enzymatic methylation reaction: methylation of CO dehydrogenase/acetyl-CoA synthase by the methylated corrinoid iron-sulfur protein J. Biol. Chem. 274, 11513-11518
26. Grahame, D. A., Khangulov, S., and Demoll, E. (1996) Reactivity of a paramagnetic enzyme-CO adduct in acetyl-CoA synthesis and cleavage Biochemistry 35, 593-600
27. Gorst, C. M. and Ragsdale, S. W. (1991) Characterization of the NiFeCO complex of carbon-monoxide dehydrogenase as a catalytically competent intermediate in the pathway of acetyl-coenzyme-A synthesis J. Biol. Chem. 266, 20687-20693
28. 2 reduction and acetyl-CoA synthesis in acetyl-CoA synthase from Clostridium thermoaceticum J. Am. Chem. Soc. 121, 9221-9222
29. Elliott, J. I. and Ljungdahl, L. G. (1982) Isolation and characterization of an Fe8-S8 ferredoxin (ferredoxin-II) from Clostridium thermoaceticum J. Bacteriol. 151, 328-333
30. Ragsdale, S. W. and Wood, H. G. (1985) Acetate biosynthesis by acetogenic bacteria - Evidence that carbon-monoxide dehydrogenase is the condensing enzyme that catalyzes the final steps of the synthesis J. Biol. Chem. 260, 3970-3977
31. Raybuck, S. A., Bastian, N. R., Ormejohnson, W. H., and Walsh, C. T. (1988) Kinetic characterization of the carbon-monoxide acetyl-CoA (carbonyl group) exchange activity of the acetyl-CoA synthesizing Co dehydrogenase from Clostridium thermoaceticum Biochemistry 27, 7698-7702
32. Lundie, L. L., Jr. and Drake, H. L. (1984) Development of a minimally defined medium for the acetogen Clostridium thermoaceticum J. Bacteriol. 159, 700-703
33. Segel, I. H. (1975) Enzyme kinetics: behavior and analysis of rapid equilibrium and steady state enzyme systems, p xxii, 957 pp, Wiley, New York.
34. Harder, S. R., Feinberg, B. A., and Ragsdale, S. W. (1989) A spectroelectrochemical cell designed for low temperature electron paramagnetic resonance titration of oxygen-sensitive proteins Anal. Biochem. 181, 283-287
35. Hinckley, G. T. and Frey, P. A. (2006) An adaptable spectroelectrochemical titrator: the midpoint reduction potential of the iron-sulfur center in lysine 2,3-aminomutase Anal. Biochem. 349, 103-111
36. Prince, R. C. and Adams, M. W. W. (1987) Oxidation-reduction properties of the 2Fe4S4 clusters in Clostridium pasteurianum ferredoxin J. Biol. Chem. 262, 5125-5128
37. Wilson, G. S. (1978) Determination of oxidation-reduction potentials Methods Enzymol. 54, 396-410
38. Dorweiler, J. S., Finke, R. G., and Matthews, R. G. (2003) Cobalamin-dependent methionine synthase: probing the role of the axial base in catalysis of methyl transfer between methyltetrahydrofolate and exogenous cob(I)alamin or cob(I)inamide Biochemistry 42, 14653-14662
39. Gao-Sheridan, H. S., Pershad, H. R., Armstrong, F. A., and Burgess, B. K. (1998) Discovery of a novel ferredoxin from Azotobacter vinelandii containing two [4Fe-4S] clusters with widely differing and very negative reduction potentials J. Biol. Chem. 273, 5514-5519
40. Green, A. J., Munro, A. W., Cheesman, M. R., Reid, G. A., von Wachenfeldt, C., and Chapman, S. K. (2003) Expression, purification and characterisation of a Bacillus subtilis ferredoxin: a potential electron transfer donor to cytochrome P450 BioI J. Inorg. Biochem. 93, 92-99
41. Yang, S. S., Ljungdahl, L. G., and Legall, J. (1977) 4-iron, 4-sulfide ferredoxin with high thermostability from Clostridium thermoaceticum J. Bacteriol. 130, 1084-1090
42. Kyritsis, P., Hatzfeld, O. M., Link, T. A., and Moulis, J. M. (1998) The two [4Fe-4S] clusters in Chromatium vinosum ferredoxin have largely different reduction potentials. Structural origin and functional consequences J. Biol. Chem. 273, 15404-15411
43. Guerrini, O., Burlat, B., Leger, C., Guigliarelli, B., Soucaille, P., and Girbal, L. (2008) Characterization of two 2[4Fe4S] ferredoxins from Clostridium acetobutylicum Curr. Microbiol. 56, 261-267
44. Mathews, R., Charlton, S., Sands, R. H., and Palmer, G. (1974) On the nature of the spin coupling between the iron-sulfur clusters in the eight-iron ferredoxins J. Biol. Chem. 249, 4326-4328
45. Mathews, R., Charlton, S., Sands, R. H., and Palmer, G. (1974) Nature of spin coupling between iron-sulfur clusters in 8-iron ferredoxins J. Biol. Chem. 249, 4326-4328
46. Saeki, K., Jain, M. K., Shen, G. J., Prince, R. C., and Zeikus, J. G. (1989) Purification and properties of ferredoxin and rubredoxin from Butyribacterium methylotrophicum J. Bacteriol. 171, 4736-4741
47. Shanmugasundaram, T. and Wood, H. G. (1992) Interaction of ferredoxin with carbon monoxide dehydrogenase from Clostridium thermoaceticum J. Biol. Chem. 267, 897-900
48. Ragsdale, S. W., Wood, H. G., and Antholine, W. E. (1985) Evidence that an iron-nickel-carbon complex is formed by reaction of CO with the CO dehydrogenase from Clostridium thermoaceticum Proc. Natl. Acad. Sci. U.S.A. 82, 6811-6814
49. Lindahl, P. A., Ragsdale, S. W., and Münck, E. (1990) Mössbauer studies of CO dehydrogenase from Clostridium thermoaceticum J. Biol. Chem. 265, 3880-3888
50. Xia, J. Q., Hu, Z. G., Popescu, C. V., Lindahl, P. A., and Munck, E. (1997) Mossbauer and EPR study of the Ni-activated alpha-subunit of carbon monoxide dehydrogenase from Clostridium thermoaceticum J. Am. Chem. Soc. 119, 8301-8312
51. Kumar, M. and Ragsdale, S. W. (1992) Characterization of the CO binding site of carbon monoxide dehydrogenase from Clostridium thermoaceticum by infrared spectroscopy J. Am. Chem. Soc. 114, 8713-8715
52. Gencic, S. and Grahame, D. A. (2003) Nickel in subunit beta of the acetyl-CoA decarbonylase/synthase multienzyme complex in methanogens: catalytic properties and evidence for a binuclear Ni-Ni site J. Biol. Chem. 278, 6101-6110
53. Bramlett, M. R., Tan, X., and Lindahl, P. A. (2003) Inactivation of acetyl-CoA synthase/carbon monoxide dehydrogenase by copper J. Am. Chem. Soc. 125, 9316-9317
54. Schenker, R. P. and Brunold, T. C. (2003) Computational studies on the A cluster of acetyl-coenzyme A synthase: geometric and electronic properties of the NiFeC species and mechanistic implications J. Am. Chem. Soc. 125, 13962-13963
55. Lu, W. P. and Ragsdale, S. W. (1991) Reductive activation of the coenzyme-A acetyl-CoA isotopic exchange-reaction catalyzed by carbon-monoxide dehydrogenase from Clostridium thermoaceticum and its inhibition by nitrous-oxide and carbon-monoxide J. Biol. Chem. 266, 3554-3564
56. Bhaskar, B., DeMoll, E., and Grahame, D. A. (1998) Redox-dependent acetyl transfer partial reaction of the acetyl-CoA decarbonylase/synthase complex: kinetics and mechanism Biochemistry 37, 14491-14499
57. Zehnder, A. J. B. and Wuhrmann, K. (1976) Titanium(III) citrate as a nontoxic oxidation-reduction buffering system for culture of obligate anaerobes Science 194, 1165-1166
58. Furdui, C. and Ragsdale, S. W. (2002) The roles of coenzyme A in the pyruvate:ferredoxin oxidoreductase reaction mechanism: rate enhancement of electron transfer from a radical intermediate to an iron-sulfur cluster Biochemistry 41, 9921-9937
59. Gencic, S. and Grahame, D. A. (2008) Two separate one-electron steps in the reductive activation of the a cluster in subunit beta of the ACDS complex in Methanosarcina thermophila Biochemistry 47, 5544-5555
60. Tan, X., Surovtsev, I. V., and Lindahl, P. A. (2006) Kinetics of CO insertion and acetyl group transfer steps, and a model of the acetyl-CoA synthase catalytic mechanism J. Am. Chem. Soc. 128, 12331-12338
61. Barondeau, D. P. and Lindahl, P. A. (1997) Methylation of carbon monoxide dehydrogenase from Clostridium thermoaceticum and mechanism of acetyl coenzyme A synthesis J. Am. Chem. Soc. 119, 3959-3970