Skip to main content
Log in

A transporter of Escherichia coli specific for l- and d-methionine is the prototype for a new family within the ABC superfamily

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

An ABC-type transporter in Escherichia coli that transports both l- and d-methionine, but not other natural amino acids, was identified. This system is the first functionally characterized member of a novel family of bacterial permeases within the ABC superfamily. This family was designated the methionine uptake transporter (MUT) family (TC #3.A.1.23). The proteins that comprise the transporters of this family were analyzed phylogenetically, revealing the probable existence of several sequence-divergent primordial paralogues, no more than two of which have been transmitted to any currently sequenced organism. In addition, MetJ, the pleiotropic methionine repressor protein, was shown to negatively control expression of the operon encoding the ABC-type methionine uptake system. The identification of MetJ binding sites (in gram-negative bacteria) or S-boxes (in gram-positive bacteria) in the promoter regions of several MUT transporter-encoding operons suggests that many MUT family members transport organic sulfur compounds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3a–c.
Fig. 4a–c.
Fig. 5a, b.

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  Google Scholar 

  • Ayling PD, Bridgeland ES (1972) Methionine transport in wild-type and transport-defective mutants of Salmonella typhimurium. J Gen Microbiol 73:127–141

    CAS  PubMed  Google Scholar 

  • Ayling PD, Mojica-a T, Klopotowski T (1979) Methionine transport in Salmonella typhimurium: evidence for at least one low-affinity transport system. J Gen Microbiol 114:227–246

    CAS  PubMed  Google Scholar 

  • Berlyn MK (1998) Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol Mol Biol Rev 62:814–984

    CAS  PubMed  Google Scholar 

  • Betteridge PR, Ayling PD (1975) The role of methionine transport-defective mutations in resistance to methionine sulphoximine in Salmonella typhimurium. Mol Gen Genet 138:41–52

    CAS  PubMed  Google Scholar 

  • Brubaker RR (1972) The genus Yersinia: biochemistry and genetics of virulence. Curr Top Microbiol Immunol 57:111–158

    CAS  PubMed  Google Scholar 

  • Chanyangam M, Smith AL, Moseley SL, Kuehn M, Jenny P (1991) Contribution of a 28-kilodalton membrane protein to the virulence of Haemophilus influenzae. Infect Immun 59:600–608

    CAS  PubMed  Google Scholar 

  • Cottam AN, Ayling PD (1989) Genetic studies of mutants in a high-affinity methionine transport system in Salmonella typhimurium. Mol Gen Genet 215:358–363

    CAS  PubMed  Google Scholar 

  • Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640–6645

    Article  CAS  PubMed  Google Scholar 

  • Gal J, Szvetnik A, Schnell R, Kalman M (2002) The metD d-methionine transporter locus of Escherichia coli is an ABC transporter gene cluster. J Bacteriol 184:4930–4932

    Article  CAS  PubMed  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    CAS  PubMed  Google Scholar 

  • Greene RC (1996) Biosynthesis of methionine. In Neidhardt FC (ed) Escherichia coli and Salmonella: cellular and molecular miology, 2nd edn, vol 1. ASM Press, Washington DC, pp. 542–560

  • Grundy CE, Ayling PD (1992) Fine structure mapping and complementation studies of the metD methionine transport system in Salmonella typhimurium. Genet Res 60:1–6

    CAS  PubMed  Google Scholar 

  • Grundy FJ, Henkin TM (1998) The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in gram-positive bacteria. Mol Microbiol 30:737–749

    Article  CAS  PubMed  Google Scholar 

  • Guzman L-M, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130

    CAS  PubMed  Google Scholar 

  • Hendricks JK, Mobley HL (1997) Helicobacter pylori ABC transporter: effect of allelic exchange mutagenesis on urease activity. J Bacteriol 179:5892–5902

    CAS  PubMed  Google Scholar 

  • Kadner RJ (1974) Transport systems for l-methionine in Escherichia coli. J Bacteriol 117:232–241

    CAS  PubMed  Google Scholar 

  • Kadner RJ (1975) Regulation of methionine transport activity in Escherichia coli. J Bacteriol 122:110–119

    CAS  PubMed  Google Scholar 

  • Kadner RJ (1977) Transport and utilization of d-methionine and other methionine sources in Escherichia coli. J Bacteriol 129:207–216

    CAS  PubMed  Google Scholar 

  • Kadner RJ, Watson WJ (1974) Methionine transport in Escherichia coli: physiological and genetic evidence for two uptake systems. J Bacteriol 119:401–409

    CAS  PubMed  Google Scholar 

  • Kadner RJ, Winkler HH (1975) Energy coupling for methionine transport in Escherichia coli. J Bacteriol 123:985–991

    CAS  PubMed  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  CAS  PubMed  Google Scholar 

  • Kuan G, Dassa E, Saurin W, Hofnung M, Saier MH Jr (1995) Phylogenetic analyses of the ATP-binding constituents of bacterial extracytoplasmic receptor-dependent ABC-type nutrient uptake permeases. Res Microbiol 146:271–278

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Blackwell TW, States DJ (2001) Conformational model for binding site recognition by the E. coli MetJ transcription factor. Bioinformatics 17:622–633

    Article  CAS  PubMed  Google Scholar 

  • Merlin C, Gardiner G, Durand S, Masters M (2002) The Escherichia coli metD locus encodes an ABC transporter which includes Abc (MetN), YaeE (MetI), and YaeC (MetQ). J Bacteriol 184:5513–5517

    Article  CAS  PubMed  Google Scholar 

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Panina EM, Mironov AA, Gelfand MS (2001) Comparative analysis of FUR regulons in gamma-proteobacteria. Nucleic Acids Res 29:5195–5206

    Article  CAS  PubMed  Google Scholar 

  • Pattery T, Hernalsteens JP, De Greve H (1999) Identification and molecular characterization of a novel Salmonella enteritidis pathogenicity islet encoding an ABC transporter. Mol Microbiol 33:791–805

    Article  CAS  PubMed  Google Scholar 

  • Poland J, Ayling PD (1984) Methionine and glutamine transport systems in d-methionine utilising revertants of Salmonella typhimurium. Mol Gen Genet 194:219–226

    CAS  PubMed  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277

    PubMed  Google Scholar 

  • Saint-Girons I, Duchange N, Cohen GN, Zakin MM (1984) Structure and autoregulation of the metJ regulatory gene in Escherichia coli. J Biol Chem 259:14282–14285

    CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Sekowska A, Kung HF, Danchin A (2000) Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol 2:145–177

    PubMed  Google Scholar 

  • Sonnhammer EL, von Heijne G, Krogh A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6:175–182

    CAS  PubMed  Google Scholar 

  • Thanbichler M, Neuhierl B, Bock A (1999) S-methylmethionine metabolism in Escherichia coli. J Bacteriol 181:662–665

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    CAS  PubMed  Google Scholar 

  • Tusnady GE, Simon I (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol 283:489–506

    CAS  PubMed  Google Scholar 

  • Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850

    Article  PubMed  Google Scholar 

  • Weissbach H, Brot N (1991) Regulation of methionine synthesis in Escherichia coli. Mol Microbiol 5:1593–1597

    PubMed  Google Scholar 

  • Yamaguchi K, Inouye M (1988) Lipoprotein 28, an inner membrane protein of Escherichia coli encoded by nlpA, is not essential for growth. J Bacteriol 170:3747–3749

    CAS  PubMed  Google Scholar 

  • Yu F, Inouye S, Inouye M (1986) Lipoprotein-28, a cytoplasmic membrane lipoprotein from Escherichia coli. Cloning, DNA sequence, and expression of its gene. J Biol Chem 261:2284–2288

    CAS  PubMed  Google Scholar 

  • Zhang Z, Aboulwafa M, Smith M, Saier MH Jr. (2003) The ascorbate transporter of Escherichia coli. J Bacteriol 185:2243–2250

    Google Scholar 

Download references

Acknowledgements

This work was supported by NIH grants GM55434 and GM64368 from the National Institute of General Medical Sciences (to MHS). JNF was supported by a Rhùne-Alpes Fellowship from France. We thank Mary Beth Hiller for her assistance in the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Milton H. Saier Jr.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Z., Feige, J.N., Chang, A.B. et al. A transporter of Escherichia coli specific for l- and d-methionine is the prototype for a new family within the ABC superfamily. Arch Microbiol 180, 88–100 (2003). https://doi.org/10.1007/s00203-003-0561-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-003-0561-4

Keywords

Navigation