1887

Abstract

Sulphate permeases in the plasma membrane are responsible for uptake of environmental sulphate used in the sulphate assimilation pathway in bacteria and plants. Here it is reported that the ORF designated , located on the chromosome between and five putative genes involved in sulphate assimilation, encodes a sulphate permease. is able to complement cysteine auxotrophs with mutations affecting either the membrane or periplasmic components of the sulphate-thiosulphate permease. Transport studies with cell suspensions of a strain transformed with a plasmid expressing the gene indicated that CysP catalyses sulphate uptake. Analysis of the primary sequence showed that CysP (354 amino acids, estimated molecular mass 24 kDa) is a highly hydrophobic protein which has 11 putative transmembrane helices. Sequence comparisons revealed that CysP, together with the phosphate permease of , Pho-4, and PitA, belongs to the family of related transporters, the inorganic phosphate transporter (Pit) family. Among the putative phosphate permeases, CysP shows a similar size and the same domain organization as the archaeal transporters. This is the first report of a sulphate permease in a Gram-positive organism.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-146-4-815
2000-04-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/146/4/1460815a.html?itemId=/content/journal/micro/10.1099/00221287-146-4-815&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden L. M., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped b last and psi-blast, a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  2. Buchel D. E., Grononborn B., Muller-Hill B. 1980; Sequence of the lactose permease gene. Nature 283:541–545 [CrossRef]
    [Google Scholar]
  3. Cervantes C., Ohtake H., Chu L., Misra T. K., Silver S. 1990; Cloning, nucleotide sequence, and expression of the chromate resistance determinant of Pseudomonas aeruginosa plasmid pUM505. J Bacteriol 172:287–291
    [Google Scholar]
  4. David S., Van der Rest M. E., Driessen A. J. M., Simons G., de Vos W. M. 1990; Nucleotide sequence and expression in Escherichia coli of the Lactococcus lactis citrate permease gene. J Bacteriol 172:5789–5794
    [Google Scholar]
  5. Hastbacka J., De La Chapelle A., Mahtani M. M.12 other authors 1994; The diastrophic dysplasia gene encodes a novel sulfate transporter: positional cloning by fine-structure linkage disequilibrium mapping. Cell 78:1073–1087 [CrossRef]
    [Google Scholar]
  6. von Heijne G. 1992; Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225:487–497 [CrossRef]
    [Google Scholar]
  7. Higgins C. F. 1992; ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113 [CrossRef]
    [Google Scholar]
  8. Hoffmann B., Strauch E., Gewinner C., Nattermann H., Appel B. 1998; Characterization of plasmid regions of foodborne Yersinia enterocolitica biogroup 1A strains hybridizing to the Yersinia enterocolitica virulence plasmid. Syst Appl Microbiol 21:201–211 [CrossRef]
    [Google Scholar]
  9. Hryniewicz M., Sirko A., Palucha A., Böck A., Hulanicka D. 1990; Sulfate and thiosulfate transport in Escherichia coli K-12: identification of a gene encoding a novel protein involved in thiosulfate binding. J Bacteriol 172:3358–3366
    [Google Scholar]
  10. Johansson P., Hederstedt L. 1999; Organization of genes for tetrapyrrole biosynthesis in Gram-positive bacteria. Microbiology 145:529–538 [CrossRef]
    [Google Scholar]
  11. Ketter J. S., Jarai G., Fu Y. H., Marzluf G. A. 1991; Nucleotide sequence, messenger RNA stability, and DNA recognition elements of cys-14, the structural gene for sulfate permease II in Neurospora crassa. J Biochem 30:1780–1787 [CrossRef]
    [Google Scholar]
  12. Kobayashi T., Sugimoto T., Saijoh K., Fukase M., Chihara K. 1997; Cloning of mouse diastrophic dysplasia sulfate transporter gene induced during osteoblast differentiation by bone morphogenetic protein-2. Gene 198:341–349 [CrossRef]
    [Google Scholar]
  13. Kredich N. M. 1996; Biosynthesis of cysteine. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp. 514–527Edited by Neidhart F. C.others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  14. Kunst F., Ogawawara N., Moszer I.148 other authors 1997; The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256 [CrossRef]
    [Google Scholar]
  15. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132 [CrossRef]
    [Google Scholar]
  16. Laudenbach D. E., Grossman A. R. 1991; Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport. J Bacteriol 173:2739–2750
    [Google Scholar]
  17. Maiden M. C. J., Davis E. O., Baldwin S. A., Moore D. C., Henderson P. J. F. 1987; Mammalian and bacterial sugar transport proteins are homologous. Nature 325:641–643 [CrossRef]
    [Google Scholar]
  18. Mann B. J., Bowman B. J., Grotelueschen J., Metzenberg R. 1989; Nucleotide sequence of pho-4 +, encoding a phosphate-repressible phosphate permease of Neurospora crassa. Gene 83:281–289 [CrossRef]
    [Google Scholar]
  19. Mansilla M. C., de Mendoza D. 1997; l-cysteine biosynthesis in Bacillus subtilis: identification, sequencing, and functional characterization of the gene coding for phosphoadenylylsulfate sulfotransferase. J Bacteriol 179:976–981
    [Google Scholar]
  20. Martinez P., Persson B. L. 1998; Identification, cloning and characterization of a derepressible Na+-coupled phosphate transporter in Saccharomyces cerevisiae. Mol Gen Genet 258:628–638 [CrossRef]
    [Google Scholar]
  21. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  22. Nakai K. 1996; Refinement of the prediction methods of signal peptides for the genome analysis of Saccharomyces cerevisiae and Bacillus subtilis. GIW-96 Genome Informatics Workshop; Tokyo: 1996 pp. 72–81 Tokyo: Universal Academy Press;
    [Google Scholar]
  23. Nies D. H., Silver S. 1989; Plasmid-determined inducible efflux is responsible for resistance to cadmium, zinc, and cobalt in Alcaligenes eutrophus. J Bacteriol 171:896–900
    [Google Scholar]
  24. Nies D. H., Koch S., Wachi S., Pietzsch N., Saier M. H. Jr 1998; CHR, a novel family of procaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J Bacteriol 180:5799–5802
    [Google Scholar]
  25. Pardee A. B., Prestidge L. S., Whipple M. B., Dreyfuss J. 1966; A binding site for sulfate and its relation to sulfate transport into Salmonella typhimurium. J Biol Chem 241:3962–3969
    [Google Scholar]
  26. Paulsen I. T., Sliwinski M. K., Saier M. H. Jr 1998; Microbial genome analyses: global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specifities. J Mol Biol 277:573–592 [CrossRef]
    [Google Scholar]
  27. Saier M. H., Eng B. H., Fard S.15 other authors 1999; Phylogenetic characterization of novel transport families revealed by genome analyses. Biochim Biophys Acta 1422:1–56 [CrossRef]
    [Google Scholar]
  28. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  29. Sirko A., Hryniewicz M., Hulanicka D., Böck A. 1990; Sulfate and thiosulfate transport in Escherichia coli K-12: nucleotide sequence and expression of the cysTWAM gene cluster. J Bacteriol 172:3351–3357
    [Google Scholar]
  30. Sirko A., Zatyka M., Sadowy E., Hulanicka D. 1995; Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate and thiosulfate-binding proteins. J Bacteriol 177:4134–4136
    [Google Scholar]
  31. Smith F. W., Ealing P. M., Hawkesford M. J., Clarkson D. T. 1995a; Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci USA 92:9373–9377 [CrossRef]
    [Google Scholar]
  32. Smith F. W., Hawkesford M. J., Prosser I. M., Clarkson D. T. 1995b; Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high affinity sulphate transporter at the plasma membrane. Mol Gen Genet 247:709–715 [CrossRef]
    [Google Scholar]
  33. Sofia H. J., Burland V., Daniels D. L., Plunkett G. III, Blattner F. R. 1994; Analysis of the Escherichia coli genome. V. DNA sequence of the region from 76·0 to 81·5 minutes. Nucleic Acids Res 22:2576–2586 [CrossRef]
    [Google Scholar]
  34. Spizizen J. 1958; Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci USA 44:1072–1078 [CrossRef]
    [Google Scholar]
  35. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. 1990; Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185:60–89
    [Google Scholar]
  36. Takahashi H., Yamazaki M., Sasakura N., Watanabe A., Leustek T., de Almeida Engler J., Engler G., Van Montagu M., Saito K. 1997; Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107 [CrossRef]
    [Google Scholar]
  37. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  38. Versaw W. K., Metzenberg R. L. 1995; Repressible cation-phosphate symporters in Neurospora crassa. Proc Natl Acad Sci USA 92:3884–3887 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-146-4-815
Loading
/content/journal/micro/10.1099/00221287-146-4-815
Loading

Data & Media loading...

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