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J Bacteriol. 1995 May; 177(10): 2813–2820.
PMCID: PMC176953

Sequence analysis of the phs operon in Salmonella typhimurium and the contribution of thiosulfate reduction to anaerobic energy metabolism.


The phs chromosomal locus of Salmonella typhimurium is essential for the dissimilatory anaerobic reduction of thiosulfate to hydrogen sulfide. Sequence analysis of the phs region revealed a functional operon with three open reading frames, designated phsA, phsB, and phsC, which encode peptides of 82.7, 21.3, and 28.5 kDa, respectively. The predicted products of phsA and phsB exhibited significant homology with the catalytic and electron transfer subunits of several other anaerobic molybdoprotein oxidoreductases, including Escherichia coli dimethyl sulfoxide reductase, nitrate reductase, and formate dehydrogenase. Simultaneous comparison of PhsA to seven homologous molybdoproteins revealed numerous similarities among all eight throughout the entire frame, hence, significant amino acid conservation among molybdoprotein oxidoreductases. Comparison of PhsB to six other homologous sequences revealed four highly conserved iron-sulfur clusters. The predicted phsC product was highly hydrophobic and similar in size to the hydrophobic subunits of the molybdoprotein oxidoreductases containing subunits homologous to phsA and phsB. Thus, phsABC appears to encode thiosulfate reductase. Single-copy phs-lac translational fusions required both anaerobiosis and thiosulfate for full expression, whereas multicopy phs-lac translational fusions responded to either thiosulfate or anaerobiosis, suggesting that oxygen and thiosulfate control of phs involves negative regulation. A possible role for thiosulfate reduction in anaerobic respiration was examined. Thiosulfate did not significantly augment the final densities of anaerobic cultures grown on any of the 18 carbon sources tested. on the other hand, washed stationary-phase cells depleted of ATP were shown to synthesize small amounts of ATP on the addition of the formate and thiosulfate, suggesting that the thiosulfate reduction plays a unique role in anaerobic energy conservation by S typhimurium.

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Selected References

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  • Barrett EL, Clark MA. Tetrathionate reduction and production of hydrogen sulfide from thiosulfate. Microbiol Rev. 1987 Jun;51(2):192–205. [PMC free article] [PubMed]
  • Berg BL, Li J, Heider J, Stewart V. Nitrate-inducible formate dehydrogenase in Escherichia coli K-12. I. Nucleotide sequence of the fdnGHI operon and evidence that opal (UGA) encodes selenocysteine. J Biol Chem. 1991 Nov 25;266(33):22380–22385. [PubMed]
  • Bilous PT, Cole ST, Anderson WF, Weiner JH. Nucleotide sequence of the dmsABC operon encoding the anaerobic dimethylsulphoxide reductase of Escherichia coli. Mol Microbiol. 1988 Nov;2(6):785–795. [PubMed]
  • Blasco F, Iobbi C, Giordano G, Chippaux M, Bonnefoy V. Nitrate reductase of Escherichia coli: completion of the nucleotide sequence of the nar operon and reassessment of the role of the alpha and beta subunits in iron binding and electron transfer. Mol Gen Genet. 1989 Aug;218(2):249–256. [PubMed]
  • Böhm R, Sauter M, Böck A. Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol. 1990 Feb;4(2):231–243. [PubMed]
  • Bokranz M, Gutmann M, Körtner C, Kojro E, Fahrenholz F, Lauterbach F, Kröger A. Cloning and nucleotide sequence of the structural genes encoding the formate dehydrogenase of Wolinella succinogenes. Arch Microbiol. 1991;156(2):119–128. [PubMed]
  • Broome-Smith JK, Ioannidis I, Edelman A, Spratt BG. Nucleotide sequences of the penicillin-binding protein 5 and 6 genes of Escherichia coli. Nucleic Acids Res. 1988 Feb 25;16(4):1617–1617. [PMC free article] [PubMed]
  • Bruschi M, Guerlesquin F. Structure, function and evolution of bacterial ferredoxins. FEMS Microbiol Rev. 1988 Apr-Jun;4(2):155–175. [PubMed]
  • Cammack R, Weiner JH. Electron paramagnetic resonance spectroscopic characterization of dimethyl sulfoxide reductase of Escherichia coli. Biochemistry. 1990 Sep 11;29(36):8410–8416. [PubMed]
  • Clark MA, Barrett EL. The phs gene and hydrogen sulfide production by Salmonella typhimurium. J Bacteriol. 1987 Jun;169(6):2391–2397. [PMC free article] [PubMed]
  • Cox DJ, Henick-Kling T. Chemiosmotic energy from malolactic fermentation. J Bacteriol. 1989 Oct;171(10):5750–5752. [PMC free article] [PubMed]
  • Ebright RH, Kolb A, Buc H, Kunkel TA, Krakow JS, Beckwith J. Role of glutamic acid-181 in DNA-sequence recognition by the catabolite gene activator protein (CAP) of Escherichia coli: altered DNA-sequence-recognition properties of [Val181]CAP and [Leu181]CAP. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6083–6087. [PMC free article] [PubMed]
  • Elliott T. A method for constructing single-copy lac fusions in Salmonella typhimurium and its application to the hemA-prfA operon. J Bacteriol. 1992 Jan;174(1):245–253. [PMC free article] [PubMed]
  • Fong CL, Heinzinger NK, Tongklan S, Barrett EL. Cloning of the phs genetic locus from Salmonella typhimurium and a role for a phs product in its own induction. J Bacteriol. 1993 Oct;175(19):6368–6371. [PMC free article] [PubMed]
  • Fürste JP, Pansegrau W, Frank R, Blöcker H, Scholz P, Bagdasarian M, Lanka E. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene. 1986;48(1):119–131. [PubMed]
  • Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem. 1988;57:199–233. [PubMed]
  • Guigliarelli B, Asso M, More C, Augier V, Blasco F, Pommier J, Giordano G, Bertrand P. EPR and redox characterization of iron-sulfur centers in nitrate reductases A and Z from Escherichia coli. Evidence for a high-potential and a low-potential class and their relevance in the electron-transfer mechanism. Eur J Biochem. 1992 Jul 1;207(1):61–68. [PubMed]
  • Hallenbeck PC, Clark MA, Barrett EL. Characterization of anaerobic sulfite reduction by Salmonella typhimurium and purification of the anaerobically induced sulfite reductase. J Bacteriol. 1989 Jun;171(6):3008–3015. [PMC free article] [PubMed]
  • Huang CJ, Barrett EL. Identification and cloning of genes involved in anaerobic sulfite reduction by Salmonella typhimurium. J Bacteriol. 1990 Jul;172(7):4100–4102. [PMC free article] [PubMed]
  • Huang CJ, Barrett EL. Sequence analysis and expression of the Salmonella typhimurium asr operon encoding production of hydrogen sulfide from sulfite. J Bacteriol. 1991 Feb;173(4):1544–1553. [PMC free article] [PubMed]
  • Kwan HS, Barrett EL. Roles for menaquinone and the two trimethylamine oxide (TMAO) reductases in TMAO respiration in Salmonella typhimurium: Mu d(Apr lac) insertion mutations in men and tor. J Bacteriol. 1983 Sep;155(3):1147–1155. [PMC free article] [PubMed]
  • O'Callaghan D, Charbit A. High efficiency transformation of Salmonella typhimurium and Salmonella typhi by electroporation. Mol Gen Genet. 1990 Aug;223(1):156–158. [PubMed]
  • Pierson DE, Campbell A. Cloning and nucleotide sequence of bisC, the structural gene for biotin sulfoxide reductase in Escherichia coli. J Bacteriol. 1990 Apr;172(4):2194–2198. [PMC free article] [PubMed]
  • Poolman B, Molenaar D, Smid EJ, Ubbink T, Abee T, Renault PP, Konings WN. Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J Bacteriol. 1991 Oct;173(19):6030–6037. [PMC free article] [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Shuber AP, Orr EC, Recny MA, Schendel PF, May HD, Schauer NL, Ferry JG. Cloning, expression, and nucleotide sequence of the formate dehydrogenase genes from Methanobacterium formicicum. J Biol Chem. 1986 Oct 5;261(28):12942–12947. [PubMed]
  • Simons RW, Houman F, Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. [PubMed]
  • Stewart V. Requirement of Fnr and NarL functions for nitrate reductase expression in Escherichia coli K-12. J Bacteriol. 1982 Sep;151(3):1320–1325. [PMC free article] [PubMed]
  • Stewart V. Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol Rev. 1988 Jun;52(2):190–232. [PMC free article] [PubMed]
  • Thauer RK, Jungermann K, Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977 Mar;41(1):100–180. [PMC free article] [PubMed]
  • Todd JA, Roberts AN, Johnstone K, Piggot PJ, Winter G, Ellar DJ. Reduced heat resistance of mutant spores after cloning and mutagenesis of the Bacillus subtilis gene encoding penicillin-binding protein 5. J Bacteriol. 1986 Jul;167(1):257–264. [PMC free article] [PubMed]
  • Voll MJ, Shiller LM, Castrilli J. His-linked hydrogen sulfide locus in Salmonella typhimurium. J Bacteriol. 1974 Nov;120(2):902–905. [PMC free article] [PubMed]
  • Weiner JH, MacIsaac DP, Bishop RE, Bilous PT. Purification and properties of Escherichia coli dimethyl sulfoxide reductase, an iron-sulfur molybdoenzyme with broad substrate specificity. J Bacteriol. 1988 Apr;170(4):1505–1510. [PMC free article] [PubMed]
  • Yamamoto I, Okubo N, Ishimoto M. Further characterization of trimethylamine N-oxide reductase from Escherichia coli, a molybdoprotein. J Biochem. 1986 Jun;99(6):1773–1779. [PubMed]
  • Zinoni F, Birkmann A, Stadtman TC, Böck A. Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4650–4654. [PMC free article] [PubMed]

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