Reassessment of the late steps of coenzyme B12 synthesis in Salmonella enterica: Evidence that dephosphorylation of adenosylcobalamin- 5′-phosphate by the CobC phosphatase is the last step of the pathway

Journal of Bacteriology

Volumn 189, Issue 6, 2007, Pages 2210-2218

  Zayas, Carmen L ^a   Escalante Semerena, Jorge C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSYLCOBALAMIN 5' PHOSPHATE; ALPHA RIBAZOLE 5' PHOSPHATE; BACTERIAL ENZYME; BENZIMIDAZOLE; COBALAMIN DERIVATIVE; COBAMAMIDE; COBINAMIDE; CORRINOID; CYANOCOBALAMIN; GUANOSINE DIPHOSPHATE; HETEROCYCLIC COMPOUND; PHOSPHATASE; PROTEIN COBC; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIOSYNTHESIS; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; SALMONELLA ENTERICA;

BACTERIAL PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COBAMIDES; CULTURE MEDIA; DNA TRANSPOSABLE ELEMENTS; MASS SPECTROMETRY; MUTAGENESIS, INSERTIONAL; PHOSPHATES; SALMONELLA TYPHIMURIUM; TRANSAMINASES;

SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 33947167675     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01665-06     Document Type: Article

References (61)

1. Atlas, R. 1995. Handbook of media for environmental microbiology. CRC Press, Boca Raton, FL.
2. Balch, W. E., and R. S. Wolfe. 1976. New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl. Environ. Microbiol. 32:781-791.
3. Berkowitz, D., J. M. Hushon, H. J. Whitfield, J. Roth, and B. N. Ames. 1968. Procedure for identifying nonsense mutations. J. Bacteriol. 96:215-220.
4. Blanche, F., L. Debussche, A. Famechon, D. Thibaut, B. Cameron, and J. Crouzet. 1991. A bifunctional protein from Pseudomonas denitrificans carries cobinamide kinase and cobinamide phosphate guanylyltransferase activities. J. Bacteriol. 173:6052-6057.
5. Blanche, F., D. Thibaut, M. Couder, and J.-C. Muller. 1990. Identification and quantitation of corrinoid precursors of cobalamin from Pseudomonas denitrificans by high-performance liquid chromatography. Anal. Biochem. 189:24-29.
6. Borths, E. L., B. Poolman, R. N. Hvorup, K. P. Locher, and D. C. Rees. 2005. In vitro functional characterization of BtuCD-F, the Escherichia coli ABC transporter for vitamin B12 uptake. Biochemistry 44:16301- 16309.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-255.
8. Brindley, A. A., E. Raux, H. K. Leech, H. L. Schubert, and M. J. Warren. 2003. A story of chelatase evolution: identification and characterization of a small 13-15-kDa "ancestral" cobaltochelatase (CbiXS) in the archaea. J. Biol. Chem. 278:22388-22395.
9. Brown, K. L. 2005. Chemistry and enzymology of vitamin B12. Chem. Rev. 105:2075-2149.
10. Buan, N. R., K. Rehfeld, and J. C. Escalante-Semerena. 2006. Studies of the CobA-type ATP:Co(I)rrinoid adenosyltransferase enzyme of Methanosarcina mazei strain Gö1. J. Bacteriol. 188:3543-3550.
11. Cadieux, N., C. Bradbeer, E. Reeger-Schneider, W. Koster, A. K. Mohanty, M. C. Wiener, and R. J. Kadner. 2002. Identification of the periplasmic cobalamin-binding protein BtuF of Escherichia coli. J. Bacteriol. 184:706-717.
12. Caetano-Annoles, G. 1993. Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl. 3:85-92.
13. Cameron, B., F. Blanche, M. C. Rouyez, D. Bisch, A. Famechon, M. Couder, L. Cauchois, D. Thibaut, L. Debussche, and J. Crouzet. 1991. Genetic analysis, nucleotide sequence, and products of two Pseudomonas denitrificans cob genes encoding nicotinate-nucleotide:dimethylbenzimidazole phosphoribosyltransferase and cobalamin (5′-phosphate) synthase. J. Bacteriol. 173:6066-6073.
14. Chan, R. K., D. Botstein, T. Watanabe, and Y. Ogata. 1972. Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high transducing lysate. Virology 50:883-898.
15. Cheong, C. G., C. B. Bauer, K. R. Brushaber, J. C. Escalante-Semerena, and I. Rayment. 2002. Three-dimensional structure of the L-threonine-O-3-phosphate decarboxylase (CobD) enzyme from Salmonella enterica. Biochemistry 41:4798-4808.
16. Cheong, C. G., J. C. Escalante-Semerena, and I. Rayment. 2002. Capture of a labile substrate by expulsion of water molecules from the active site of nicotinate mononucleotide:5,6-dimethylbenzimidazole phosphoribosyltransferase (CobT) from Salmonella enterica. J. Biol. Chem. 277:41120-41127.
17. Cheong, C. G., J. C. Escalante-Semerena, and I. Rayment. 2001. Structural investigation of the biosynthesis of alternative lower ligands for cobamides by nicotinate mononucleotide:5,6-dimethylbenzimidazole phosphoribosyltransferase from Salmonella enterica. J. Biol. Chem. 276:37612-37620.
18. Cheong, C. G., J. C. Escalante-Semerena, and I. Rayment. 1999. The three-dimensional structures of nicotinate mononucleotide:5,6- dimethylbenzimidazole phosphoribosyltransferase (CobT) from Salmonella typhimurium complexed with 5,6-dimethybenzimidazole and its reaction products determined to 1.9 Å resolution. Biochemistry 38:16125-16135.
19. Davis, R. W., D. Botstein, and J. R. Roth. 1980. A manual for genetic engineering: advanced bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. 12 transport in Escherichia coli. J. Bacteriol. 167:920-927.
21. Drennan, C. L., S. Huang, J. T. Drummond, R. G. Matthews, and M. L. Ludwig. 1994. How a protein binds B12: a 3.0A X-ray structure of B12-binding domains of methionine synthase. Science 266:1660-1674.
22. Elliott, T., and J. R. Roth. 1988. Characterization of Tn10d-Cam: a transposition-defective Tn10 specifying chloramphenicol resistance. Mol. Gen. Genet. 213:332-338.
23. Escalante-Semerena, J. C., and J. R. Roth. 1987. Regulation of cobalamin biosynthetic operons in Salmonella typhimurium. J. Bacteriol. 169:2251-2258.
24. Escalante-Semerena, J. C., S. J. Sun, and J. R. Roth. 1990. cobA function is required for both de novo cobalamin biosynthesis and assimilation of exogcorrinoids in Salmonella typhimurium. J. Bacteriol. 172:273-280.
25. Friedmann, H. C. 1968. Vitamin B12 biosynthesis. Evidence for a new precursor vitamin B12 5′-phosphate. J. Biol. Chem. 243:2065-2075.
26. 12. Proc. Natl. Acad. Sci. USA, in press.
27. Hall, D. A., C. W. Vander Kooi, C. N. Stasik, S. Y. Stevens, E. R. Zuiderweg, and R. G. Matthews. 2001. Mapping the interactions between flavodoxin and its physiological partners flavodoxin reductase and cobalamin-dependent methionine synthase. Proc. Natl. Acad. Sci. USA 98:9521-9526.
28. 12 receptor protein in the outer membrane of Escherichia coli. J. Bacteriol. 161:904-908.
29. Heller, K., B. J. Mann, and R. J. Kadner. 1985. Cloning and expression of the gene for the vitamin B12 receptor protein in the outer membrane of Escherichia coli. J. Bacteriol. 161:896-903.
30. Jeter, R. M., B. M. Olivera, and J. R. Roth. 1984. Salmonella typhimurium synthesizes cobalamin (vitamin B12) de novo under anaerobic growth conditions. J. Bacteriol. 159:206-213.
31. Johnson, M. G., and J. C. Escalante-Semerena. 1992. Identification of 5,6-dimethylbenzimidazole as the Co? ligand of the cobamide synthesized by Salmonella typhimurium. Nutritional characterization of mutants defective in biosynthesis of the imidazole ring. J. Biol. Chem. 267:13302-13305.
32. Keck, B., M. Munder, and P. Renz. 1998. Biosynthesis of cobalamin in Salmonella typhimurium: transformation of riboflavin into the 5,6-dimethylbenzimidazole moiety. Arch. Microbiol. 171:66-68.
33. Keck, B., and P. Renz. 2000. Salmonella typhimurium forms adenylcobamide and 2-methyladenylcobamide, but no detectable cobalamin during strictly anaerobic growth. Arch. Microbiol. 173:76-77.
34. Maggio-Hall, L. A., and J. C. Escalante-Semerena. 2003. Alpha-5,6-dimethylbenzimidazole adenine dinucleotide (alpha-DAD), a putative new intermediate of coenzyme B12 biosynthesis in Salmonella typhimurium. Microbiology 149:983-990.
35. Maggio-Hall, L. A., and J. C. Escalante-Semerena. 1999. In vitro synthesis of the nucleotide loop of cobalamin by Salmonella typhimurium enzymes. Proc. Natl. Acad. Sci. USA 96:11798-11803.
36. Miroux, B., and J. E. Walker. 1996. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260:289-298.
37. O'Toole, G. A., and J. C. Escalante-Semerena. 1995. Purification and characterization of the bifunctional CobU enzyme of Salmonella typhimurium LT2. Evidence for a CobU-GMP intermediate. J. Biol. Chem. 270:23560- 23569.
38. O'Toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
39. O'Toole, G. A., M. R. Rondon, and J. C. Escalante-Semerena. 1993. Analysis of mutants of Salmonella typhimurium defective in the synthesis of the nucleotide loop of cobalamin. J. Bacteriol. 175:3317-3326.
40. O'Toole, G. A., J. R. Trzebiatowski, and J. C. Escalante-Semerena. 1994. The cobC gene of Salmonella typhimurium codes for a novel phosphatase involved in the assembly of the nucleotide loop of cobalamin. J. Biol. Chem. 269:26503-26511.
41. Peariso, K., Z. S. Zhou, A. E. Smith, R. G. Matthews, and J. E. Penner-Hahn. 2001. Characterization of the zinc sites in cobalamin-independent and cobalamin-dependent methionine synthase using zinc and selenium X-ray absorption spectroscopy. Biochemistry 40:987-993.
42. Rioux, C. R., and R. J. Kadner. 1989. Vitamin B12 transport in Escherichia coli K12 does not require the btuE gene of the btuCED operon. Mol. Gen. Genet. 217:301-308.
43. Rodionov, D. A., A. G. Vitreschak, A. A. Mironov, and M. S. Gelfand. 2003. Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J. Biol. Chem. 278:41148-41159.
44. Roth, J. R., J. G. Lawrence, and T. A. Bobik. 1996. Cobalamin (coenzyme B12): synthesis and biological significance. Annu. Rev. Microbiol. 50:137-181.
45. Schmieger, H. 1971. A method for detection of phage mutants with altered transduction ability. Mol. Gen. Genet. 100:378-381.
46. Schmieger, H., and H. Bakhaus. 1973. The origin of DNA in transducing particles of P22 mutants with increased transduction frequencies (HT-mutants). Mol. Gen. Genet. 120:181-190.
47. Scott, A. I. 2003. Discovering nature's diverse pathways to vitamin B12: a 35-year odyssey. J. Org. Chem. 68:2529-2539.
48. Suh, S.-J., and J. C. Escalante-Semerena. 1995. Purification and initial characterization of the ATP:corrinoid adenosyltransferase encoded by the cobA gene of Salmonella typhimurium. J. Bacteriol. 177:921-925.
49. Tabor, S. 1990. Expression using the T7 RNA polymerase/promoter system, p. 16.2.1.-16.2.11. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 2. Wiley Interscience, New York, NY.
50. Taylor, R. T., and H. Weissbach. 1973. N5- methylenetetrahydrofolate-homocysteine methyltransferases, p. 121-165. In P. D. Boyer (ed.), The enzymes, vol. 9. Academic Press, Inc., New York, NY.
51. Thomas, M. G., and J. C. Escalante-Semerena. 2000. Identification of an alternative nucleoside triphosphate:5′- deoxyadenosylcobinamide phosphate nucleotidyltransferase in Methanobacterium thermoautotrophicum ΔH. J. Bacteriol. 182:4227-4233.
52. Trzebiatowski, J. R., and J. C. Escalante-Semerena. 1997. Purification and characterization of CobT, the nicotinate mononucleotide:5,6- dimethylbenzimidazole phosphoribosyltransferase enzyme from Salmonella typhimurium LT2. J. Biol. Chem. 272:17662-17667.
53. 1-(5-phospho-α-D-ribosyl)-5,6- dimethylbenzimidazole, an intermediate in the synthesis of the nucleotide loop of cobalamin. J. Bacteriol. 176:3568-3575.
54. Tsang, A. W., and J. C. Escalante-Semerena. 1998. CobB, a new member of the SIR2 family of eucaryotic regulatory proteins, is required to compensate for the lack of nicotinate mononucleotide:5,6-dimethylbenzimidazole phosphoribosyltransferase activity in cobT mutants during cobalamin biosynthesis in Salmonella typhimurium LT2. J. Biol. Chem. 273:31788-31794.
55. Van Bibber, M., C. Bradbeer, N. Clark, and J. R. Roth. 1999. A new class of cobalamin transport mutants (btuF) provides genetic evidence for a periplasmic binding protein in Salmonella typhimurium. J. Bacteriol. 181:5539-5541.
56. Vogel, H. J., and D. M. Bonner. 1956. Acetylornithase of Escherichia coli: partial purification, and some properties. J. Biol. Chem. 218:97-106.
57. Warren, M. J., E. Raux, H. L. Schubert, and J. C. Escalante-Semerena. 2002. The biosynthesis of adenosylcobalamin (vitamin B12). Nat. Prod. Rep. 19: 390-412.
58. Way, J. C., M. A. Davis, D. Morisato, D. E. Roberts, and N. Kleckner. 1984. New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene 32:369-379.
59. Woodson, J. D., and J. C. Escalante-Semerena. 2004. CbiZ, an amidohydrolase enzyme required for salvaging the coenzyme B12 precursor cobinamide in archaea. Proc. Natl. Acad. Sci. USA 101:3591-3596.
60. Woodson, J. D., R. F. Peck, M. P. Krebs, and J. C. Escalante-Semerena. 2003. The cobY gene of the archaeon Halobacterium sp. strain NRC-1 is required for de novo cobamide synthesis. J. Bacteriol. 185:311-316.
61. 12 precursor cobinamide in archaea requires cobinamide-phosphate synthase (CbiB) enzyme activity. J. Bacteriol. 185:7193-7201.