1887

Abstract

Several cellular pathways have been identified which affect the efficiency of thiamine biosynthesis in . Mutants defective in iron–sulfur (Fe–S) cluster metabolism are less efficient at synthesis of the pyrimidine moiety of thiamine. These mutants are compromised for the conversion of aminoimidazole ribotide (AIR) to 4-amino-5-hydroxymethyl-2-methylpyrimidine phosphate (HMP-P), not the synthesis of AIR. The gene product ThiC contains potential ligands for an Fe–S cluster that are required for function . The conversion of AIR to HMP-P is sensitive to oxidative stress, and variants of ThiC have been identified that have increased sensitivity to oxidative growth conditions. The data are consistent with ThiC or an as-yet-unidentified protein involved in HMP-P synthesis containing an Fe–S cluster required for its physiological function.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28926-0
2006-08-01
2020-04-09
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/8/2345.html?itemId=/content/journal/micro/10.1099/mic.0.28926-0&mimeType=html&fmt=ahah

References

  1. Allen S, Zilles J. L, Downs D. M. 2002; Metabolic flux in both the purine mononucleotide and histidine biosynthetic pathways can influence synthesis of the hydroxymethyl pyrimidine moiety of thiamine in Salmonella enterica . J Bacteriol184:6130–6137[CrossRef]
    [Google Scholar]
  2. Bartolome B, Jubete Y, Martinez E, de la Cruz F. 1991; Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene102:75–78[CrossRef]
    [Google Scholar]
  3. Beck B. J, Downs D. M. 1998; The apbE gene encodes a lipoprotein involved in thiamine synthesis in Salmonella typhimurium . J Bacteriol180:885–891
    [Google Scholar]
  4. Benov L, Fridovich I. 1999; Why superoxide imposes an aromatic amino acid auxotrophy on Escherichia coli . The transketolase connection. J Biol Chem274:4202–4206[CrossRef]
    [Google Scholar]
  5. Benov L, Kredich N. M, Fridovich I. 1996; The mechanism of the auxotrophy for sulfur-containing amino acids imposed upon Escherichia coli by superoxide. J Biol Chem271:21037–21040[CrossRef]
    [Google Scholar]
  6. Bhat B, Groziak M. P, Leonard N. J. 1990; Nonenzymatic synthesis and properties of 5-aminoimidazole ribonucleotide (AIR). Synthesis of specifically [sup]15[/sup]N-labeled 5-aminoimidazole ribonucleoside (AIRs) derivatives. J Am Chem Soc112:4891–4897[CrossRef]
    [Google Scholar]
  7. Carlioz A, Touati D. 1986; Isolation of superoxide dismutase mutants in Escherichia coli : is superoxide dismutase necessary for aerobic life?. EMBO J5:623–630
    [Google Scholar]
  8. Castilho B. A, Olfson P, Casadaban M. J. 1984; Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol158:488–495
    [Google Scholar]
  9. Chabriere E, Charon M. H, Volbeda A, Pieulle L, Hatchikian E. C, Fontecilla-Camps J. C. 1999; Crystal structures of the key anaerobic enzyme pyruvate : ferredoxin oxidoreductase, free and in complex with pyruvate. Nat Struct Biol6:182–190[CrossRef]
    [Google Scholar]
  10. Charon M. H, Volbeda A, Chabriere E, Pieulle L, Fontecilla-Camps J. C. 1999; Structure and electron transfer mechanism of pyruvate : ferredoxin oxidoreductase. Curr Opin Struct Biol9:663–669[CrossRef]
    [Google Scholar]
  11. Cui Q, Thorgersen M. P, Westler W. M, Markley J. L, Downs D. M. 2006; Solution structure of YggX: a prokaryotic protein involved in Fe(II) trafficking. Proteins62:578–586
    [Google Scholar]
  12. Datsenko K. A, Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A97:6640–6645[CrossRef]
    [Google Scholar]
  13. Davis R. W, Botstein D, Roth J. R. Cold Spring Harbor Laboratory 1980; Advanced Bacterial Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  14. Dougherty M, Downs D. M. 2003; The stm4066 gene product of Salmonella enterica serovar Typhimurium has aminoimidazole riboside (AIRs) kinase activity and allows AIRs to satisfy the thiamine requirement of pur mutant strains. J Bacteriol185:332–339[CrossRef]
    [Google Scholar]
  15. Dougherty M. J, Downs D. M. 2004; A mutant allele of rpoD results in increased conversion of aminoimidazole ribotide to hydroxymethyl pyrimidine in Salmonella enterica . J Bacteriol186:4034–4037[CrossRef]
    [Google Scholar]
  16. Downs D. M, Petersen L. 1994; apbA , a new genetic locus involved in thiamine biosynthesis in Salmonella typhimurium . J Bacteriol176:4858–4864
    [Google Scholar]
  17. Estramareix B, David S. 1990; Conversion of 5-aminoimidazole ribotide to the pyrimidine of thiamin in enterobacteria: study of the pathway with specifically labeled samples of riboside. Biochim Biophys Acta1035:154–160[CrossRef]
    [Google Scholar]
  18. Estramareix B, Therisod M. 1984; Biosynthesis of thiamin: 5-aminoimidazole as the precursor of all the carbon atoms of the pyrimidine moiety. J Am Chem Soc106:3857–3860[CrossRef]
    [Google Scholar]
  19. Flint D. H, Smyk-Randall E, Tuminello J. F, Draczynska-Lusiak B, Brown O. R. 1993; The inactivation of dihydroxy-acid dehydratase in Escherichia coli treated with hyperbaric oxygen occurs because of the destruction of its Fe–S cluster, but the enzyme remains in the cell in a form that can be reactivated. J Biol Chem268:25547–25552
    [Google Scholar]
  20. Frodyma M. E, Downs D. 1998; ApbA, the ketopantoate reductase enzyme of Salmonella typhimurium is required for the synthesis of thiamine via the alternative pyrimidine biosynthetic pathway. J Biol Chem273:5572–5576[CrossRef]
    [Google Scholar]
  21. Frodyma M, Rubio A, Downs D. M. 2000; Reduced flux through the purine biosynthetic pathway results in an increased requirement for coenzyme A in thiamine synthesis in Salmonella enterica serovar Typhimurium. J Bacteriol182:236–240[CrossRef]
    [Google Scholar]
  22. Gralnick J, Downs D. 2001; Protection from superoxide damage associated with an increased level of the YggX protein in Salmonella enterica . Proc Natl Acad Sci U S A98:8030–8035[CrossRef]
    [Google Scholar]
  23. Gralnick J, Webb E, Beck B, Downs D. 2000; Lesions in gshA (encoding gamma-l-glutamyl-l-cysteine synthetase) prevent aerobic synthesis of thiamine in Salmonella enterica serovar typhimurium LT2. J Bacteriol182:5180–5187[CrossRef]
    [Google Scholar]
  24. Guzman L. M, Belin D, Carson M. J, Beckwith J. 1995; Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol177:4121–4130
    [Google Scholar]
  25. Harlow E, Lane D. 1999; Using Antibodies: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  26. Hassan H. M. 1984; Exacerbation of superoxide radical formation by paraquat. Methods Enzymol105:523–532
    [Google Scholar]
  27. Kuo C, Mashino T, Fridovich I. 1987; α , β -Dihydroxyisovalerate dehydratase. A superoxide-sensitive enzyme. J Biol Chem262:4724–4727
    [Google Scholar]
  28. Lawhorn B. G, Mehl R. A, Begley T. P. 2004; Biosynthesis of the thiamin pyrimidine: the reconstitution of a remarkable rearrangement reaction. Org Biomol Chem2:2538–2546[CrossRef]
    [Google Scholar]
  29. Leonardi R, Fairhurst S. A, Kriek M, Lowe D. J, Roach P. L. 2003; Thiamine biosynthesis in Escherichia coli : isolation and initial characterisation of the ThiGH complex. FEBS Lett539:95–99[CrossRef]
    [Google Scholar]
  30. Martinez-Gomez N. C, Robers M, Downs D. M. 2004; Mutational analysis of ThiH, a member of the radical S -adenosylmethionine (AdoMet) protein superfamily. J Biol Chem279:40505–40510[CrossRef]
    [Google Scholar]
  31. Petersen L, Enos-Berlage J, Downs D. M. 1996; Genetic analysis of metabolic crosstalk and its impact on thiamine synthesis in Salmonella typhimurium . Genetics143:37–44
    [Google Scholar]
  32. Pieulle L, Guigliarelli B, Asso M, Dole F, Bernadac A, Hatchikian E. C. 1995; Isolation and characterization of the pyruvate-ferredoxin oxidoreductase from the sulfate-reducing bacterium Desulfovibrio africanus . Biochim Biophys Acta1250:49–59[CrossRef]
    [Google Scholar]
  33. Pieulle L, Magro V, Hatchikian E. C. 1997; Isolation and analysis of the gene encoding the pyruvate-ferredoxin oxidoreductase of Desulfovibrio africanus , production of the recombinant enzyme in Escherichia coli , and effect of carboxy-terminal deletions on its stability. J Bacteriol179:5684–5692
    [Google Scholar]
  34. Skovran E, Downs D. M. 2000; Metabolic defects caused by mutations in the isc gene cluster in Salmonella enterica serovar Typhimurium: implications for thiamine synthesis. J Bacteriol182:3896–3903[CrossRef]
    [Google Scholar]
  35. Skovran E, Downs D. M. 2003; Lack of the ApbC or ApbE protein results in a defect in Fe–S cluster metabolism in Salmonella enterica serovar Typhimurium. J Bacteriol185:98–106[CrossRef]
    [Google Scholar]
  36. Skovran E, Lauhon C. T, Downs D. M. 2004; Lack of YggX results in chronic oxidative stress and uncovers subtle defects in Fe–S cluster metabolism in Salmonella enterica . J Bacteriol186:7626–7634[CrossRef]
    [Google Scholar]
  37. Sofia H. J, Chen G, Hetzler B. G, Reyes-Spindola J. F, Miller N. E. 2001; Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res29:1097–1106[CrossRef]
    [Google Scholar]
  38. Vander Horn P. B, Backstrom A. D, Stewart V, Begley T. P. 1993; Structural genes for thiamine biosynthetic enzymes (thiCEFGH) in Escherichia coli K-12. J Bacteriol175:982–992
    [Google Scholar]
  39. Vogel H. J, Bonner D. M. 1956; Acetylornithinase of Escherichia coli : partial purification and some properties. J Biol Chem218:97–106
    [Google Scholar]
  40. Way J. C, Davis M. A, Morisato D, Roberts D. E, Kleckner N. 1984; New Tn 10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene32:369–379[CrossRef]
    [Google Scholar]
  41. Zhang Y, Begley T. P. 1997; Cloning, sequencing and regulation of thiA , a thiamin biosynthesis gene from Bacillus subtilis . Gene198:73–82[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28926-0
Loading
/content/journal/micro/10.1099/mic.0.28926-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error