Enzymatic and electron paramagnetic resonance studies of anabolic pyruvate synthesis by pyruvate: Ferredoxin oxidoreductase from Hydrogenobacter thermophilus

FEBS Journal

Volumn 277, Issue 2, 2010, Pages 501-510

  Ikeda, Takeshi ^a,c   Yamamoto, Masahiro ^a   Arai, Hiroyuki ^a   Ohmori, Daijiro ^b   Ishii, Masaharu ^a   Igarashi, Yasuo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JUNTENDO UNIVERSITY   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Hydrogenobacter thermophilus; Iron sulfur cluster; Pyruvate: ferredoxin oxidoreductase; Reductive tricarboxylic acid cycle; Thiamine pyrophosphate

Indexed keywords

1,3 DITHIANE DERIVATIVE; 2 (1 HYDROXYETHYLIDENE) THIAMINEPYROPHOSPHATE; 2 OXOGLUTARIC ACID; ACETYL COENZYME A; CARBON DIOXIDE; FERREDOXIN; OXIDOREDUCTASE; PYROPHOSPHATE; PYRUVATE SYNTHASE; PYRUVIC ACID; REDUCING AGENT; THIAMINE PYROPHOSPHATASE; UNCLASSIFIED DRUG;

AEROBIC BACTERIUM; ARTICLE; CARBOXYLATION; CATALYSIS; CHEMICAL REACTION; CITRIC ACID CYCLE; ELECTRON SPIN RESONANCE; ENERGY; ENZYME ANALYSIS; ENZYME SYNTHESIS; HYDROGENOBACTER THERMOPHILUS; NONHUMAN; PRIORITY JOURNAL;

ACETYL COENZYME A; BACTERIA; BACTERIAL PROTEINS; CARBON DIOXIDE; CITRIC ACID CYCLE; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENERGY METABOLISM; KETONE OXIDOREDUCTASES; KINETICS; L-LACTATE DEHYDROGENASE; PYRUVATE SYNTHASE; PYRUVIC ACID; RECOMBINANT PROTEINS;

BACTERIA (MICROORGANISMS); HYDROGENOBACTER THERMOPHILUS;

EID: 74549131687     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07506.x     Document Type: Article

References (57)

1. Kerscher L Oesterhelt D (1982) Pyruvate: ferredoxin oxidoreductase - new findings on an ancient enzyme. Trends Biochem Sci 7, 371 374.
2. Kawasumi T, Igarashi Y, Kodama T Minoda Y (1984) Hydrogenobacter thermophilus gen. nov., sp. nov., an extremely thermophilic, aerobic, hydrogen-oxidizing bacterium. Int J Syst Bacteriol 34, 5 10.
3. Pitulle C, Yang Y, Marchiani M, Moore ERB, Siefert JL, Aragno M, Jurtshuk P Jr. Fox GE (1994) Phylogenetic position of the genus Hydrogenobacter. Int J Syst Bacteriol 44, 620 626.
4. 2 assimilation via the reductive tricarboxylic acid cycle in an obligately autotrophic, aerobic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus. Arch Microbiol 141, 198 203.
5. 2 fixation pathways in archaea (Crenarchaeota). Arch Microbiol 179, 160 173.
6. Evans MCW, Buchanan BB Arnon DI (1966) A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc Natl Acad Sci USA 55, 928 934.
7. Buchanan BB Arnon DI (1990) A reverse KREBS cycle in photosynthesis: consensus at last. Photosynth Res 24, 47 53.
8. Ikeda T, Yamamoto M, Arai H, Ohmori D, Ishii M Igarashi Y (2005) Two tandemly arranged ferredoxin genes in the Hydrogenobacter thermophilus genome: comparative characterization of the recombinant [4Fe-4S] ferredoxins. Biosci Biotechnol Biochem 69, 1172 1177.
9. Adams MWW Kletzin A (1996) Oxidoreductase-type enzymes and redox proteins involved in fermentative metabolisms of hyperthermophilic archaea. Adv Protein Chem 48, 101 180. (Pubitemid 126686821)
10. Drake HL, Hu S-I Wood HG (1981) Purification of five components from Clostridium thermoaceticum which catalyze synthesis of acetate from pyruvate and methyltetrahydrofolate. Properties of phosphotransacetylase. J Biol Chem 256, 11137 11144.
11. Pieulle L, Guigliarelli B, Asso M, Dole F, Bernadac A Hatchikian EC (1995) Isolation and characterization of the pyruvate-ferredoxin oxidoreductase from the sulfate-reducing bacterium Desulfovibrio africanus. Biochim Biophys Acta 1250, 49 59.
12. Kerscher L Oesterhelt D (1981) Purification and properties of two 2-oxoacid: ferredoxin oxidoreductases from Halobacterium halobium. Eur J Biochem 116, 587 594.
13. Zhang Q, Iwasaki T, Wakagi T Oshima T (1996) 2-oxoacid: ferredoxin oxidoreductase from the thermoacidophilic archaeon, Sulfolobus sp. strain 7. J Biochem 120, 587 599.
14. Blamey JM Adams MWW (1994) Characterization of an ancestral type of pyruvate ferredoxin oxidoreductase from the hyperthermophilic bacterium, Thermotoga maritima. Biochemistry 33, 1000 1007.
15. Kletzin A Adams MWW (1996) Molecular and phylogenetic characterization of pyruvate and 2-ketoisovalerate ferredoxin oxidoreductases from Pyrococcus furiosus and pyruvate ferredoxin oxidoreductase from Thermotoga maritima. J Bacteriol 178, 248 257.
16. Yun N-R, Yamamoto M, Arai H, Ishii M Igarashi Y (2002) A novel five-subunit-type 2-oxoglutarate: ferredoxin oxidoreductase from Hydrogenobacter thermophilus TK-6. Biochem Biophys Res Commun 292, 280 286.
17. Ikeda T, Ochiai T, Morita S, Nishiyama A, Yamada E, Arai H, Ishii M Igarashi Y (2006) Anabolic five subunit-type pyruvate: ferredoxin oxidoreductase from Hydrogenobacter thermophilus TK-6. Biochem Biophys Res Commun 340, 76 82.
18. Deckert G, Warren PV, Gaasterland T, Young WG, Lenox AL, Graham DE, Overbeek R, Snead MA, Keller M, Aujay M et al. (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392, 353 358.
19. Chabrière E, Charon M-H, Volbeda A, Pieulle L, Hatchikian EC Fontecilla-Camps J-C (1999) Crystal structures of the key anaerobic enzyme pyruvate: ferredoxin oxidoreductase, free and in complex with pyruvate. Nat Struct Biol 6, 182 190.
20. Ragsdale SW (2003) Pyruvate ferredoxin oxidoreductase and its radical intermediate. Chem Rev 103, 2333 2346.
21. Tittmann K (2009) Reaction mechanisms of thiamin diphosphate enzymes: redox reactions. FEBS J 276, 2454 2468.
22. Thauer RK, Jungermann K Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41, 100 180.
23. Furdui C Ragsdale SW (2000) The role of pyruvate ferredoxin oxidoreductase in pyruvate synthesis during autotrophic growth by the Wood-Ljungdahl pathway. J Biol Chem 275, 28494 28499.
24. Yoon K-S, Hille R, Hemann C Tabita FR (1999) Rubredoxin from the green sulfur bacterium Chlorobium tepidum functions as an electron acceptor for pyruvate ferredoxin oxidoreductase. J Biol Chem 274, 29772 29778.
25. Yoon K-S, Bobst C, Hemann CF, Hille R Tabita FR (2001) Spectroscopic and functional properties of novel 2[4Fe-4S] cluster-containing ferredoxins from the green sulfur bacterium Chlorobium tepidum. J Biol Chem 276, 44027 44036.
26. Ueda Y, Yamamoto M, Urasaki T, Arai H, Ishii M Igarashi Y (2007) Sequencing and reverse transcription-polymerase chain reaction (RT-PCR) analysis of four hydrogenase gene clusters from an obligately autotrophic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus TK-6. J Biosci Bioeng 104, 470 475.
27. Tersteegen A Hedderich R (1999) Methanobacterium thermoautotrophicum encodes two multisubunit membrane-bound [NiFe] hydrogenases. Transcription of the operons and sequence analysis of the deduced proteins. Eur J Biochem 264, 930 943.
28. Taguchi H, Yamashita M, Matsuzawa H Ohta T (1982) Heat-stable and fructose 1,6-bisphosphate-activated l-lactate dehydrogenase from an extremely thermophilic bacterium. J Biochem 91, 1343 1348.
29. Robb FT, Park J-B Adams MWW (1992) Characterization of an extremely thermostable glutamate dehydrogenase: a key enzyme in the primary metabolism of the hyperthermophilic archaebacterium, Pyrococcus furiosus. Biochim Biophys Acta 1120, 267 272.
30. Yoon K-S, Ishii M, Igarashi Y Kodama T (1996) Purification and characterization of 2-oxoglutarate: ferredoxin oxidoreductase from a thermophilic, obligately chemolithoautotrophic bacterium, Hydrogenobacter thermophilus TK-6. J Bacteriol 178, 3365 3368.
31. Beinert H Thomson AJ (1983) Three-iron clusters in iron-sulfur proteins. Arch Biochem Biophys 222, 333 361.
32. Blamey JM Adams MWW (1993) Purification and characterization of pyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus. Biochim Biophys Acta 1161, 19 27.
33. Mai X Adams MWW (1994) Indolepyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus. A new enzyme involved in peptide fermentation. J Biol Chem 269, 16726 16732.
34. Ozawa Y, Nakamura T, Kamata N, Yasujima D, Urushiyama A, Yamakura F, Ohmori D Imai T (2005) Thermococcus profundus 2-ketoisovalerate ferredoxin oxidoreductase, a key enzyme in the archaeal energy-producing amino acid metabolic pathway. J Biochem 137, 101 107.
35. Uyeda K Rabinowitz JC (1971) Pyruvate-ferredoxin oxidoreductase. IV. Studies on the reaction mechanism. J Biol Chem 246, 3120 3125.
36. Menon S Ragsdale SW (1997) Mechanism of the Clostridium thermoaceticum pyruvate: Ferredoxin oxidoreductase: evidence for the common catalytic intermediacy of the hydroxyethylthiamine pyrophosphate radical. Biochemistry 36, 8484 8494.
37. Chabrière E, Vernède X, Guigliarelli B, Charon M-H, Hatchikian EC Fontecilla-Camps JC (2001) Crystal structure of the free radical intermediate of pyruvate: ferredoxin oxidoreductase. Science 294, 2559 2563.
38. Mansoorabadi SO, Seravalli J, Furdui C, Krymov V, Gerfen GJ, Begley TP, Melnick J, Ragsdale SW Reed GH (2006) EPR spectroscopic and computational characterization of the hydroxyethylidene-thiamine pyrophosphate radical intermediate of pyruvate: ferredoxin oxidoreductase. Biochemistry 45, 7122 7131.
39. Frank RAW, Kay CWM, Hirst J Luisi BF (2008) Off-pathway, oxygen-dependent thiamine radical in the Krebs cycle. J Am Chem Soc 130, 1662 1668.
40. Cammack R, Kerscher L Oesterhelt D (1980) A stable free radical intermediate in the reaction of 2-oxoacid: ferredoxin oxidoreductases of Halobacterium halobium. FEBS Lett 118, 271 273.
41. Bock A-K, Schönheit P Teixeira M (1997) The iron-sulfur centers of the pyruvate: ferredoxin oxidoreductase from Methanosarcina barkeri (Fusaro). FEBS Lett 414, 209 212.
42. Kerscher L Oesterhelt D (1981) The catalytic mechanism of 2-oxoacid: ferredoxin oxidoreductases from Halobacterium halobium. One-electron transfer at two distinct steps of the catalytic cycle. Eur J Biochem 116, 595 600.
43. Sticht H Rösch P (1998) The structure of iron-sulfur proteins. Prog Biophys Mol Biol 70, 95 136.
44. Gehring U Arnon DI (1972) Purification and properties of α-ketoglutarate synthase from a photosynthetic bacterium. J Biol Chem 247, 6963 6969.
45. Yamamoto M, Ikeda T, Arai H, Ishii M Igarashi Y (2009) Carboxylation reaction catalyzed by 2-oxoglutarate: ferredoxin oxidoreductases from Hydrogenobacter thermophlius. Extremophiles doi :.
46. + reductase from the thermophilic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus TK-6. FEMS Microbiol Lett 297, 124 130.
47. Kameya M, Ikeda T, Nakamura M, Arai H, Ishii M Igarashi Y (2007) A novel ferredoxin-dependent glutamate synthase from the hydrogen-oxidizing chemoautotrophic bacterium Hydrogenobacter thermophilus TK-6. J Bacteriol 189, 2805 2812.
48. Schneider G Lindqvist Y (1998) Crystallography and mutagenesis of transketolase: mechanistic implications for enzymatic thiamin catalysis. Biochim Biophys Acta 1385, 387 398.
49. Furdui C Ragsdale SW (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.
50. Yoon K-S, Ishii M, Kodama T Igarashi Y (1997) Carboxylation reactions of pyruvate: Ferredoxin oxidoreductase and 2-oxoglutarate: ferredoxin oxidoreductase from Hydrogenobacter thermophilus TK-6. Biosci Biotechnol Biochem 61, 510 513.
51. Yoon K-S, Ishii M, Kodama T Igarashi Y (1997) Purification and characterization of pyruvate: ferredoxin oxidoreductase from Hydrogenobacter thermophilus TK-6. Arch Microbiol 167, 275 279.
52. Yamamoto M, Arai H, Ishii M Igarashi Y (2003) Characterization of two different 2-oxoglutarate: ferredoxin oxidoreductases from Hydrogenobacter thermophilus TK-6. Biochem Biophys Res Commun 312, 1297 1302.
53. Koide S, Iwata S, Matsuzawa H Ohta T (1991) Crystallization of allosteric l-lactate dehydrogenase from Thermus caldophilus and preliminary crystallographic data. J Biochem 109, 6 7.
54. Chen J-S Blanchard DK (1979) A simple hydrogenase-linked assay for ferredoxin and flavodoxin. Anal Biochem 93, 216 222.
55. Moreno SNJ, Mason RP, Muniz RPA, Cruz FS Docampo R (1983) Generation of free radicals from metronidazole and other nitroimidazoles by Tritrichomonas foetus. J Biol Chem 258, 4051 4054.
56. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82, 70 77.
57. Barletta G, Chung AC, Rios CB, Jordan F Schlegel JM (1990) Electrochemical oxidation of enamines related to the key intermediate on thiamin diphosphate dependent enzymatic pathways: evidence for one-electron oxidation via a thiazolium cation radical. J Am Chem Soc 112, 8144 8149.