Epimerase (Msed_0639) and Mutase (Msed_0638 and Msed_2055) convert (S)-methylmalonyl-coenzyme a (CoA) to Succinyl-coA in the Metallosphaera sedula 3-Hydroxypropionate/4-hydroxybutyrate cycle

Applied and Environmental Microbiology

Volumn 78, Issue 17, 2012, Pages 6194-6202

  Han, Yejun ^a   Hawkins, Aaron S ^a   Adams, Michael W W ^b   Kelly, Robert M ^a  

^a North Carolina State University   (United States)

^b University of Georgia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING MOTIF; CARBON DIOXIDE FIXATION; CATALYTIC SUBUNITS; CO2 FIXATION; COEXPRESSED; DIVALENT CATION; HETEROTETRAMERS; HETEROTROPHIC GROWTH; HOMODIMERS; METAL BINDING; METHYLMALONYL-COA MUTASE; OPTIMAL TEMPERATURE; ORTHOLOGS; SEQUENCE ALIGNMENTS; SPECIFIC ACTIVITY;

CARBON DIOXIDE; ENCODING (SYMBOLS); ESCHERICHIA COLI; GENE ENCODING; GENE EXPRESSION;

ENZYMES;

ACYL COENZYME A; CARBON DIOXIDE; COBAMAMIDE; HYDROXYBUTYRIC ACID; ISOMERASE; METHYLMALONYL COENZYME A MUTASE; METHYLMALONYL COENZYME A RACEMASE; METHYLMALONYL-COENZYME A; METHYLMALONYL-COENZYME A RACEMASE; METHYLMALONYLCOENZYME A; RECOMBINANT PROTEIN; SUCCINYL COENZYME A; SUCCINYL-COENZYME A;

AUTOTROPHY; CARBON DIOXIDE; CATALYSIS; ENZYME ACTIVITY; GENE EXPRESSION; GENOME; GROWTH RATE; HETEROTROPHY; PROKARYOTE;

ARTICLE; AUTOTROPHY; BIOTRANSFORMATION; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; HETEROTROPHY; METABOLISM; PROTEIN MULTIMERIZATION; SULFOLOBALES;

ACYL COENZYME A; AUTOTROPHIC PROCESSES; BIOTRANSFORMATION; CARBON DIOXIDE; COBAMIDES; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION PROFILING; HETEROTROPHIC PROCESSES; HYDROXYBUTYRATES; METHYLMALONYL-COA MUTASE; PROTEIN MULTIMERIZATION; RACEMASES AND EPIMERASES; RECOMBINANT PROTEINS; SULFOLOBACEAE;

CRENARCHAEOTA; ESCHERICHIA COLI; METALLOSPHAERA SEDULA; SULFOLOBACEAE;

EID: 84864719159     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01312-12     Document Type: Article

References (56)

1. 2 fixation. J. Bacteriol. 190:1383-1389. doi:10.1128/JB.01593-07.
2. Allen SHG, Kellermeyer R, Stjernholm R, Jacobson B, Wood HG. 1963. The isolation, purification, and properties of methylmalonyl racemase. J. Biol. Chem. 238:1637-1642.
3. Allen SHG, Kellermeyer RW, Stjernholm RL, Wood HG. 1964. Purification and properties of enzymes involved in the propionic acid fermentation. J. Bacteriol. 87:171-187.
4. Auernik KS, Kelly RM. 2010. Impact of molecular hydrogen on chalcopyrite bioleaching by the extremely thermoacidophilic archaeon Metallosphaera sedula. Appl. Environ. Microbiol. 76:2668-2672.
5. Auernik KS, Kelly RM. 2010. Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by transcriptomic analysis of heterotrophic, autotrophic, and mixotrophic growth. Appl. Environ. Microbiol. 76:931-935.
6. Auernik KS, Maezato Y, Blum PH, Kelly RM. 2008. The genome sequence of the metal-mobilizing, extremely thermoacidophilic archaeon Metallosphaera sedula provides insights into bioleaching-associated metabolism. Appl. Environ. Microbiol. 74:682-692.
7. Banerjee R, Ragsdale SW. 2003. The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes. Annu. Rev. Biochem. 72:209-247. doi:10.1146/annurev.biochem.72.121801.161828.
8. Bar-Even A, Noor E, Lewis NE, Milo R. 2010. Design and analysis of synthetic carbon fixation pathways. Proc. Natl. Acad. Sci. U. S. A. 107:8889-8894.
9. Berg IA, Kockelkorn D, Buckel W, Fuchs G. 2007. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318:1782-1786. doi:10.1126/science.1149976.
10. Berg IA, et al. 2010. Autotrophic carbon fixation in archaea. Nat. Rev. Microbiol. 8:447-460.
11. Birch A, Leiser A, Robinson JA. 1993. Cloning, sequencing, and expression of the gene encoding methylmalonyl-coenzymeAmutase from Streptomyces cinnamonensis. J. Bacteriol. 175:3511-3519.
12. Bobik TA, Rasche ME. 2003. HPLC assay for methylmalonyl-CoA epimerase. Anal. Bioanal. Chem. 375:344-349.
13. Bobik TA, Rasche ME. 2001. Identification of the human methylmalonyl-CoA racemase gene based on the analysis of prokaryotic gene arrangements. J. Biol. Chem. 276:37194-37198.
14. Bobik TA, Rasche ME. 2004. Purification and partial characterization of the Pyrococcus horikoshii methylmalonyl-CoA epimerase. Appl. Microbiol. Biotechnol. 63:682-685.
15. Cracan V, Padovani D, Banerjee R. 2010. IcmF is a fusion between the radical B12 enzyme isobutyryl-CoA mutase and its G-protein chaperone. J. Biol. Chem. 285:655-666.
16. Drennan CL, Huang S, Drummond JT, Matthews RG, Lidwig ML. 1994. How a protein binds B12: a 3.0 A X-ray structure of B12-binding domains of methionine synthase. Science 266:1669-1674. doi:10.1126/science.7992050.
17. Estelmann S, et al. 2011. Labeling and enzyme studies of the central carbon metabolism in Metallosphaera sedula. J. Bacteriol. 193:1191-1200. doi:10.1128/JB.01155-10.
18. Eswar N, et al. 2003. Tools for comparative protein structure modeling and analysis. Nucleic Acids Res. 31:3375-3380. doi:10.1093/nar/gkg543.
19. Eswar N, et al. 2007. Comparative protein structure modeling using Modeller. Curr. Protoc. Protein Sci. 50:2.9.1-2.9.31.
20. Fenton WA, Hack AM, Willard HF, Gertler A, Rosenberg LE. 1982. Purification and properties of methylmalonyl coenzyme A mutase from human liver. Arch. Biochem. Biophys. 214:815-823.
21. Froese DS, et al. 2010. Structures of the human GTPase MMAA and vitamin B12-dependent methylmalonyl-CoA mutase and insight into their complex formation. J. Biol. Chem. 285:38204-38213.
22. Fuchs G. 2011. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu. Rev. Microbiol. 65:631-658. doi:10.1146/annurev-micro-090110-102801.
23. Gruber K, Kratky C. 2001. Methylmalonyl CoA mutase, p 995-1009. In Messerschmidt A, Huber R, Poulos T, Wieghardt K (ed), Handbook of metallosproteins. John Wiley & Sons, Ltd., Chichester, United Kingdom.
24. Han Y, et al. 2010. Comparative analyses of two thermophilic enzymes exhibiting both β-1,4 mannosidic and β-1,4 glucosidic cleavage activities from Caldanaerobius polysaccharolyticus. J. Bacteriol. 192:4111-4121. doi: 10.1128/JB.00257-10.
25. Hawkins AS, et al. 2011. Extremely thermophilic routes to microbial electrofuels. ACS Catal. 1:1043-1050. doi:10.1021/cs2003017.
26. Holloway DE, Marsh EN. 1994. Adenosylcobalamin-dependent glutamate mutase from Clostridium tetanomorphum. Overexpression in Escherichia coli, purification, and characterization of the recombinant enzyme. J. Biol. Chem. 269:20425-20430.
27. Huber G, Spinnler C, Gambacorta A, Stetter KO. 1989. Metallosphaera sedula gen. and sp. nov. represents a new genus of aerobic, metalmobilizing, thermoacidophilic archaebacteria. Syst. Appl. Microbiol. 12:38-47.
28. Hügler M, Krieger RS, Jahn M, Fuchs G. 2003. Characterization of acetyl-CoA/propionyl-CoA carboxylase in Metallosphaera sedula. Eur. J. Biochem. 270:736-744.
29. Kamoun P. 1992. Valine is a precursor of propionyl-CoA. Trends Biochem. Sci. 17:175-176.
30. Kockelkorn D, Fuchs G. 2009. Malonic semialdehyde reductase, succinic semialdehyde reductase, and succinyl-coenzyme A reductase from Metallosphaera sedula: enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in Sulfolobales. J. Bacteriol. 191:6352-6362. doi:10.1128/JB.00794-09.
31. Korotkova N, Chistoserdova L, Kuksa V, Lidstrom ME. 2002. Glyoxylate regeneration pathway in the methylotroph Methylobacterium extorquens AM1. J. Bacteriol. 184:1750-1758. doi:10.1128/JB.184.6.1750-1758.2002.
32. Korotkova N, Lidstrom ME. 2004. MeaB is a component of the methyl-malonyl-CoA mutase complex required for protection of the enzyme from inactivation. J. Biol. Chem. 279:13652-13658.
33. Kühnl J, et al. 2005. Functional analysis of the methylmalonyl CoA epimerase from Caenorhabditis elegans. FEBS J. 272:1465-1477. doi:10.1111/j.1742-4658.2005.04579.x.
34. Leadlay PF. 1981. Purification and characterization of methylmalonyl-CoA epimerase from Propionibacterium shermanii. Biochemical J. 197:413-419.
35. Maiti N, Widjaja L, Banerjee R. 1999. Proton transfer from histidine 244 may facilitate the 1,2 rearrangement reaction in coenzyme B12-dependent methylmalonyl-CoA mutase. J. Biol. Chem. 274:32733-32737.
36. Mancia F, et al. 1996. How coenzyme B12 radicals are generated: the crystal structure of methylmalonyl-coenzyme A mutase at 2 Å resolution. Structure 4:339-350.
37. Marsh EN, Harding SE. 1993. Methylmalonyl-CoA mutase from Propionibacterium shermanii: characterization of the cobalamin-inhibited form and subunit-cofactor interactions studied by analytical ultracentrifugation. Biochem. J. 290:551-555.
38. Marsh EN, Harding SE, Leadlay PF. 1989. Subunit interactions in Propionibacterium shermanii methylmalonyl-CoA mutase studied by analytical ultracentrifugation. Biochem. J. 260:353-358.
39. Marsh EN, McKie N, Davis NK, Leadlay PF. 1989. Cloning and structural characterization of the genes coding for adenosylcobalamindependent methylmalonyl-CoA mutase from Propionibacterium shermanii. Biochem. J. 260:345-352.
40. Marsh ENG, Holloway DE. 1992. Cloning and sequencing of glutamate mutase component S from Clostridium tetanomorphum Homologies with other cobalamin-dependent enzymes. FEBS Lett. 310:167-170. doi: 10.1016/0014-5793(92)81321-C.
41. McCarthy AA, et al. 2001. Expression, crystallization and preliminary characterization of methylmalonyl coenzyme A epimerase from Propionibacterium shermanii. Acta Crystallogr. D Biol. Crystallogr. 57(Pt 5):706-708.
42. McCarthy AA, Baker HM, Shewry SC, Patchett ML, Baker EN. 2001. Crystal structure of methylmalonyl-coenzyme A epimerase from P. shermanii: a novel enzymatic function on an ancient metal binding scaffold. Structure 9:637-646.
43. McKie N, Keep NH, Patchett ML, Leadlay PF. 1990. Adenosylcobalamin-dependent methylmalonyl-CoA mutase from Propionibacterium shermanii. Active holoenzyme produced from Escherichia coli. Biochem. J. 269:293-298.
44. Menendez C, Bauer Z, Huber H, Stetter KO, Fuchs G. 1999. Presence of acetyl coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J. Bacteriol. 181:1088-1098.
45. Miyamoto E, et al. 2010. Characterization of methylmalonyl-CoA mutase involved in the propionate photoassimilation of Euglena gracilis Z. Arch. Microbiol. 192:437-446.
46. Miyamoto E, et al. 2003. Purification and characterization of homodimeric methylmalonyl-CoA mutase from Sinorhizobium meliloti. Arch. Microbiol. 180:151-154.
47. Miyamoto E, Watanabe F, Yamaguchi Y, Takenaka H, Nakano Y. 2004. Purification and characterization of methylmalonyl-CoA mutase from a photosynthetic coccolithophorid alga, Pleurochrysis carterae. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 138:163-167.
48. Miyamoto E, et al. 2002. Purification and characterization of methylmalonyl-CoA mutase from a methanol-utilizing bacterium, Methylobacterium extorquens NR-1. J. Nutr. Sci. Vitaminol. 48:242-246. doi:10.3177/jnsv.48.242.
49. Ogata H, et al. 1999. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27:29-34. doi:10.1093/nar/27.1.29.
50. Ramos-Vera WH, Weiss M, Strittmatter E, Kockelkorn D, Fuchs G. 2011. Identification of missing genes and enzymes for autotrophic carbon fixation in Crenarchaeota. J. Bacteriol. 193:1201-1211. doi:10.1128/JB.01156-10.
51. Ratnatilleke A, Vrijbloed JW, Robinson JA. 1999. Cloning and sequencing of the coenzyme B12-binding domain of isobutyryl-CoA mutase from Streptomyces cinnamonensis, reconstitution of mutase activity, and characterization of the recombinant rnzyme produced in Escherichia coli. J. Biol. Chem. 274:31679-31685.
52. Shi L, Gao P, Yan XX, Liang DC. 2009. Crystal structure of a putative methylmalonyl coenzyme a epimerase from Thermoanaerobacter tengcongensis at 2.0 Å resolution. Proteins 77:994-999. doi:10.1002/prot.22528.
53. Stabler SP, Marcell PD, Allen RH. 1985. Isolation and characterization of methylmalonyl-coenzyme A racemase from rat liver. Arch. Biochem. Biophys. 241:252-264.
54. Teufel R, Kung JW, Kockelkorn D, Alber BE, Fuchs G. 2009. 3-Hydroxypropionyl-coenzyme A dehydratase and acryloyl-coenzyme A reductase, enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in the Sulfolobales. J. Bacteriol. 191:4572-4581. doi:10.1128/JB.00068-09.
55. Wilkemeyer MF, Crane AM, Ledley FD. 1990. Primary structure and activity of mouse methylmalonyl-CoA mutase. Biochem. J. 271:449-455.
56. Zagalak B, Retey J, Sund H. 1974. Studies on methylmalonyl-CoA mutase from Propionibacterium shermanii. Eur. J. Biochem. 44:529-535.