• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Sep 1996; 178(18): 5438–5446.
PMCID: PMC178364

Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source.


Genes whose expression is regulated by sulfate starvation in Escherichia coli were identified by generating random translational lacZ fusions in the chromosome with the lambda placMu9 system. Nine lacZ fusion strains which expressed beta-galactosidase after growth under sulfate starvation conditions but not after growth in the presence of sulfate were found. These included two strains with insertions in the dmsA and rhsD genes, respectively, and seven strains in which the insertions were located within a 1.8-kb region downstream of hemB at 8.5 minutes on the E. coli chromosome. Analysis of the nucleotide sequence of this region indicated the presence of four open reading frames designated tauABCD. Disruption of these genes resulted in the loss of the ability to utilize taurine (2-aminoethanesulfonate) as a source of sulfur but did not affect the utilization of a range of other aliphatic sulfonates as sulfur sources. The TauA protein contained a putative signal peptide for transport into the periplasm; the TauB and TauC proteins showed sequence similarity to ATP-binding proteins and membrane proteins, respectively, of ABC-type transport systems; and the TauD protein was related in sequence to a dichlorophenoxyacetic acid dioxygenase. We therefore suggest that the proteins encoded by tauABC constitute an uptake system for taurine and that the product of tauD is involved in the oxygenolytic release of sulfite from taurine. The transcription initiation site was detected 26 to 27 bp upstream of the translational start site of tauA. Expression of the tauD gene was dependent on CysB, the transcriptional activator of the cysteine regulon.

Full Text

The Full Text of this article is available as a PDF (388K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ames GF, Mimura CS, Shyamala V. Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: Traffic ATPases. FEMS Microbiol Rev. 1990 Aug;6(4):429–446. [PubMed]
  • Babst M, Hennecke H, Fischer HM. Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum. Mol Microbiol. 1996 Feb;19(4):827–839. [PubMed]
  • Beil S, Kehrli H, James P, Staudenmann W, Cook AM, Leisinger T, Kertesz MA. Purification and characterization of the arylsulfatase synthesized by Pseudomonas aeruginosa PAO during growth in sulfate-free medium and cloning of the arylsulfatase gene (atsA). Eur J Biochem. 1995 Apr 15;229(2):385–394. [PubMed]
  • Bergler H, Högenauer G, Turnowsky F. Sequences of the envM gene and of two mutated alleles in Escherichia coli. J Gen Microbiol. 1992 Oct;138(10):2093–2100. [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]
  • Bremer E, Silhavy TJ, Weinstock GM. Transposable lambda placMu bacteriophages for creating lacZ operon fusions and kanamycin resistance insertions in Escherichia coli. J Bacteriol. 1985 Jun;162(3):1092–1099. [PMC free article] [PubMed]
  • Butler JD, Levin SW, Facchiano A, Miele L, Mukherjee AB. Amino acid composition and N-terminal sequence of purified cystine binding protein of Escherichia coli. Life Sci. 1993;52(14):1209–1215. [PubMed]
  • Casadaban MJ. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976 Jul 5;104(3):541–555. [PubMed]
  • Cotter PA, Gunsalus RP. Oxygen, nitrate, and molybdenum regulation of dmsABC gene expression in Escherichia coli. J Bacteriol. 1989 Jul;171(7):3817–3823. [PMC free article] [PubMed]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [PMC free article] [PubMed]
  • Elkins MF, Earhart CF. Nucleotide sequence and regulation of the Escherichia coli gene for ferrienterobactin transport protein FepB. J Bacteriol. 1989 Oct;171(10):5443–5451. [PMC free article] [PubMed]
  • Fu C, Parker J. A ribosomal frameshifting error during translation of the argI mRNA of Escherichia coli. Mol Gen Genet. 1994 May 25;243(4):434–441. [PubMed]
  • Fukumori F, Hausinger RP. Purification and characterization of 2,4-dichlorophenoxyacetate/alpha-ketoglutarate dioxygenase. J Biol Chem. 1993 Nov 15;268(32):24311–24317. [PubMed]
  • Green LS, Grossman AR. Changes in sulfate transport characteristics and protein composition of Anacystis nidulans R2 during sulfur deprivation. J Bacteriol. 1988 Feb;170(2):583–587. [PMC free article] [PubMed]
  • Hawley DK, McClure WR. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 1983 Apr 25;11(8):2237–2255. [PMC free article] [PubMed]
  • Hellinga HW, Evans PR. Nucleotide sequence and high-level expression of the major Escherichia coli phosphofructokinase. Eur J Biochem. 1985 Jun 3;149(2):363–373. [PubMed]
  • Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113. [PubMed]
  • Huxtable RJ. Physiological actions of taurine. Physiol Rev. 1992 Jan;72(1):101–163. [PubMed]
  • Iwanicka-Nowicka R, Hryniewicz MM. A new gene, cbl, encoding a member of the LysR family of transcriptional regulators belongs to Escherichia coli cys regulon. Gene. 1995 Dec 1;166(1):11–17. [PubMed]
  • Kertesz MA. Desulfonation of aliphatic sulfonates by Pseudomonas aeruginosa PAO. FEMS Microbiol Lett. 1996 Apr 1;137(2-3):221–225. [PubMed]
  • Kertesz MA, Leisinger T, Cook AM. Proteins induced by sulfate limitation in Escherichia coli, Pseudomonas putida, or Staphylococcus aureus. J Bacteriol. 1993 Feb;175(4):1187–1190. [PMC free article] [PubMed]
  • Klein P, Kanehisa M, DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. [PubMed]
  • Kohara Y, Akiyama K, Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. [PubMed]
  • Kondo H, Ishimoto M. Purification and properties of sulfoacetaldehyde sulfo-lyase, a thiamine pyrophosphate-dependent enzyme forming sulfite and acetate. J Biochem. 1975 Aug;78(2):317–325. [PubMed]
  • Kondo H, Kagotani K, Oshima M, Ishimoto M. Purification and some properties of taurine dehydrogenase from a bacterium. J Biochem. 1973 Jun;73(6):1269–1278. [PubMed]
  • Fraga D, Fillingame RH. Essential residues in the polar loop region of subunit c of Escherichia coli F1F0 ATP synthase defined by random oligonucleotide-primed mutagenesis. J Bacteriol. 1991 Apr;173(8):2639–2643. [PMC free article] [PubMed]
  • Mazel D, Marlière P. Adaptive eradication of methionine and cysteine from cyanobacterial light-harvesting proteins. Nature. 1989 Sep 21;341(6239):245–248. [PubMed]
  • McLaggan D, Epstein W. Escherichia coli accumulates the eukaryotic osmolyte taurine at high osmolarity. FEMS Microbiol Lett. 1991 Jun 15;65(2):209–213. [PubMed]
  • Mytelka DS, Chamberlin MJ. Escherichia coli fliAZY operon. J Bacteriol. 1996 Jan;178(1):24–34. [PMC free article] [PubMed]
  • Nicholson ML, Laudenbach DE. Genes encoded on a cyanobacterial plasmid are transcriptionally regulated by sulfur availability and CysR. J Bacteriol. 1995 Apr;177(8):2143–2150. [PMC free article] [PubMed]
  • Norrander J, Kempe T, Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. [PubMed]
  • O'Neill GP, Thorbjarnardóttir S, Michelsen U, Pálsson S, Söll D, Eggertsson G. delta-Aminolevulinic acid dehydratase deficiency can cause delta-aminolevulinate auxotrophy in Escherichia coli. J Bacteriol. 1991 Jan;173(1):94–100. [PMC free article] [PubMed]
  • Quirk PG, Guffanti AA, Clejan S, Cheng J, Krulwich TA. Isolation of Tn917 insertional mutants of Bacillus subtilis that are resistant to the protonophore carbonyl cyanide m-chlorophenylhydrazone. Biochim Biophys Acta. 1994 Jun 28;1186(1-2):27–34. [PubMed]
  • Sadosky AB, Davidson A, Lin RJ, Hill CW. rhs gene family of Escherichia coli K-12. J Bacteriol. 1989 Feb;171(2):636–642. [PMC free article] [PubMed]
  • Sadosky AB, Gray JA, Hill CW. The RhsD-E subfamily of Escherichia coli K-12. Nucleic Acids Res. 1991 Dec;19(25):7177–7183. [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]
  • Saurin W, Dassa E. Sequence relationships between integral inner membrane proteins of binding protein-dependent transport systems: evolution by recurrent gene duplications. Protein Sci. 1994 Feb;3(2):325–344. [PMC free article] [PubMed]
  • Shi X, Bennett GN. Effects of rpoA and cysB mutations on acid induction of biodegradative arginine decarboxylase in Escherichia coli. J Bacteriol. 1994 Nov;176(22):7017–7023. [PMC free article] [PubMed]
  • Shimamoto G, Berk RS. Catabolism of taurine in Pseudomonas aeruginosa. Biochim Biophys Acta. 1979 Aug 15;569(2):287–292. [PubMed]
  • Shimamoto G, Berk RS. Taurine catabolism. II. biochemical and genetic evidence for sulfoacetaldehyde sulfo-lyase involvement. Biochim Biophys Acta. 1980 Sep 17;632(1):121–130. [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]
  • Smillie DA, Hayward RS, Suzuki T, Fujita N, Ishihama A. Locations of genes encoding alkyl hydroperoxide reductase on the physical map of the Escherichia coli K-12 genome. J Bacteriol. 1992 Jun;174(11):3826–3827. [PMC free article] [PubMed]
  • Streber WR, Timmis KN, Zenk MH. Analysis, cloning, and high-level expression of 2,4-dichlorophenoxyacetate monooxygenase gene tfdA of Alcaligenes eutrophus JMP134. J Bacteriol. 1987 Jul;169(7):2950–2955. [PMC free article] [PubMed]
  • Thöny B, Hennecke H. The -24/-12 promoter comes of age. FEMS Microbiol Rev. 1989 Dec;5(4):341–357. [PubMed]
  • Toyama S, Soda K. Occurrence of taurine: -ketoglutarate aminotransferase in bacterial extracts. J Bacteriol. 1972 Feb;109(2):533–538. [PMC free article] [PubMed]
  • Trun NJ, Silhavy TJ. Characterization and in vivo cloning of prlC, a suppressor of signal sequence mutations in Escherichia coli K12. Genetics. 1987 Aug;116(4):513–521. [PMC free article] [PubMed]
  • Uria-Nickelsen MR, Leadbetter ER, Godchaux W., 3rd Sulphonate utilization by enteric bacteria. J Gen Microbiol. 1993 Feb;139(2):203–208. [PubMed]
  • Uria-Nickelsen MR, Leadbetter ER, Godchaux W., 3rd Sulfonate-sulfur utilization involves a portion of the assimilatory sulfate reduction pathway in Escherichia coli. FEMS Microbiol Lett. 1994 Oct 15;123(1-2):43–48. [PubMed]
  • Vieira J, Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. [PubMed]
  • von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. [PMC free article] [PubMed]
  • Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. [PMC free article] [PubMed]
  • Weiner JH, Rothery RA, Sambasivarao D, Trieber CA. Molecular analysis of dimethylsulfoxide reductase: a complex iron-sulfur molybdoenzyme of Escherichia coli. Biochim Biophys Acta. 1992 Aug 28;1102(1):1–18. [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...