1887

Abstract

SUMMARY: Operons encoding homologous arsenic-resistance determinants (ars) have been discovered in bacterial plasmids from Gram-positive and Gram-negative, organisms, as well as in the Escherichia coli chromosome. However, evidence for this arsenic-resistance determinant in the medically and environmentally important bacterial species Pseudomonas aeruginosa is conflicting. Here the identification of a P. aeruginosa chromosomal ars operon homologue via cloning and complementation of an E. coli ars mutant is reported. The P. aeruginosa chromosomal ars operon contains three potential ORFs encoding proteins with significant sequence similarity to those encoded by the arsR, arsB and arsC genes of the plasmid-based and E. coli chromosomal ars operons. The cloned P. aeruginosa chromosomal ars operon confers augmented resistance to arsenic and antimony oxyanions in an E. coli arsB mutant and in wild-type P. aeruginosa. Expression of the operon was induced by arsenite at the mRNA level. DNA sequences homologous with this operon were detected in some, but not all, species of the genus Pseudomonas, suggesting that its conservation follows their taxonomic-based evolution.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-144-10-2705
1998-10-01
2024-10-03
Loading full text...

Full text loading...

/deliver/fulltext/micro/144/10/mic-144-10-2705.html?itemId=/content/journal/micro/10.1099/00221287-144-10-2705&mimeType=html&fmt=ahah

References

  1. Autexier C., DuBow M.S. 1992; The Escherichia coli Mu/D108 phage ner homologue gene (nlp) is transcribed and evolutionarily conserved among the Enterobacteriaceae.. Gene 114:13–18
    [Google Scholar]
  2. Barnes W.M. 1977; Plasmid detection and sizing in single colony lysates.. Science 195:393–394
    [Google Scholar]
  3. Bröer S., Ji G., Bröer A., Silver S. 1993; Arsenic efflux governed by the arsenic resistance determinant of Staphylococcus aureus plasmid pI258.. J Bacteriol 175:3480–3485
    [Google Scholar]
  4. Bruhn D.F., Li J., Silver S., Roverto F., Rosen B.P. 1996; The arsenical resistance operon of IncN plasmid R46.. FEMS Microbiol Lett 139:149–153
    [Google Scholar]
  5. Cai J., DuBow M.S. 1996; Expression of the Escherichia coli chromosomal ars operon.. Can J Microbiol 42:662–671
    [Google Scholar]
  6. Cai J., DuBow M.S. 1997; Use of a luminescent bacterial biosensor for biomonitoring and characterization of arsenic toxicity in chromated copper arsenate.. Biodegradation 8:97–103
    [Google Scholar]
  7. Carlin A., Shi W., Dey S., Rosen B.P. 1995; The ars operon of Escherichia coli confers arsenical and antimonial resistance.. J Bacteriol 177:981–986
    [Google Scholar]
  8. Cervante C., Chávez J. 1992; Plasmid-determined resistance to arsenic and antimony in Pseudomonas aeruginosa. . Antonie Leeuwenhoek 61:333–337
    [Google Scholar]
  9. Chang J.T., Green C.B.-R., Wolf R.E. JR 1995; Inhibition of translation on Escherichia coli gnd mRNA by formation of a long-range secondary structure involving the ribosome binding site and the internal complementary sequence.. J Bacteriol 177:6560–6567
    [Google Scholar]
  10. Chen Y., Rosen B.P. 1997; Metalloregulatory properties of the ArsD repressor.. J Biol Chem 272:14257–14262
    [Google Scholar]
  11. Chen C.M., Misra T.K., Silver S., Rosen B.P. 1986; Nucleotide sequence of the structural genes for an anion pump: the plasmid-encoded arsenical resistance operon.. J Biol Chem 261:15030–15038
    [Google Scholar]
  12. Chen H., Bjerknes M., Kumar R., Jay E. 1994; Determination of the optimal aligned spacing between the Shine-Dalgarno sequence and the translation initiation codon of Escherichia coli mRNAs.. Nucleic Acids Res 22:4953–4957
    [Google Scholar]
  13. Darzins A., Casadaban M.J. 1989; Mini-D3112 bacteriophage transposable elements for genetic analysis of Pseudomonas aeruginosa. . J Bacteriol 171:3909–3916
    [Google Scholar]
  14. Dey S., Rosen B.P. 1995; Dual mode of energy coupling by the oxyanion translocating ArsB protein.. J Bacteriol 177:385–389
    [Google Scholar]
  15. Diorio C., Cai J., Marmor J., Shinder R., DuBow M.S. 1995; An Escherichia coli chromosomal ars operon homolog is functional in arsenic detoxification and conserved in Gram-negative bacteria.. J Bacteriol 177:2050–2056
    [Google Scholar]
  16. Eisenberg D., Schwarz E., Komaromy M., Wall R. 1984; Analysis of membrane and surface protein sequences with the hydrophobic moment plot.. J Mol Biol 179:125–142
    [Google Scholar]
  17. Farinha M.A., Kropinski A.M. 1990; High efficiency electroporation of Pseudomonas aeruginosa using frozen cell suspensions.. FEMS Microbiol Lett 58:221–225
    [Google Scholar]
  18. Gladysheva T.B., Oden K.L., Rosen B.P. 1994; Properties of the arsenate reductase of plasmid R773.. Biochemistry 33:7288–7293
    [Google Scholar]
  19. Higgins D.G., Sharp P.M. 1988; CLUSTAL: a package for performing multiple sequence alignment on a microcomputer.. Gene 73:237–244
    [Google Scholar]
  20. Higgins D.G., Sharp P.M. 1989; Fast and sensitive multiple sequence alignments on a microcomputer.. Comput Appl Biosci 5:151–153
    [Google Scholar]
  21. Huang H., Huang C.F., Wu D.R., Jinn C.M., Jan K.Y. 1993; Glutathione as a cellular defence against arsenite toxicity in cultured Chinese hamster ovary cells.. Toxicology 79:195–204
    [Google Scholar]
  22. Huckle J.W., Morby A.P., Turner J.S., Robinson N.J. 1993; Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions.. Mol Microbiol 7:177–187
    [Google Scholar]
  23. Ji G., Silver S. 1992a; Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258.. Proc Natl Acad Sci USA 89:9474–9478
    [Google Scholar]
  24. Ji G., Silver S. 1992b; Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258.. J Bacteriol 174:3684–3694
    [Google Scholar]
  25. Ji G., Garber E.A.E., Armes L.G., Chen C.M., Fuchs J.A., Silver S. 1994; Arsenate reductase of Staphylococcus aureus pI258.. Biochemistry 33:7294–7299
    [Google Scholar]
  26. Kaur P., Rosen B.P. 1992; Plasmid-encoded resistance to arsenic and antimony.. Plasmid 27:29–10
    [Google Scholar]
  27. Kaur P., Rosen B.P. 1994a; Identification of the site of [ɑ- 32P]ATP adduct formation in the ArsA protein.. Biochemistry 33:6456–6461
    [Google Scholar]
  28. Kaur P., Rosen B.P. 1994b; In vitro assembly of an anion- stimulated ATPase from peptide fragments.. J Biol Chem 269:9698–9704
    [Google Scholar]
  29. Li J., Liu S., Rosen B.P. 1996; Interaction of ATP binding sites in the ArsA ATPase, the catalytic subunit of the Ars pump. . J Biol Chem 271:25247–25252
    [Google Scholar]
  30. Miller J.H. 1972 Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  31. Minamishima Y., Takeya K., Ohnishi Y., Amako K. 1968; Physicochemical and biological properties of fibrous Pseudomonas bacteriophages.. J Virol 2:208–213
    [Google Scholar]
  32. Mobley H.L.T., Rosen B.P. 1982; Energetics of plasmidmediated arsenate resistance in Escherichia coli. . Proc Natl Acad Sci USA 79:6119–6122
    [Google Scholar]
  33. Myers E.W., Miller W. 1988; Optimal alignments in linear space.. Comput Appl Biosci 4:11–17
    [Google Scholar]
  34. Neyt C, Iriarte M., Thi V.H., Cornells G.R. 1997; Virulence and arsenic resistance in Yersiniae. . J Bacteriol 179:612–619
    [Google Scholar]
  35. Oden K.L., Gladysheva T.B., Rosen B.P. 1994; Arsenate reduction mediated by the plasmid-encoded ArsC protein is coupled to glutathione.. Mol Microbiol 12:301–306
    [Google Scholar]
  36. Owolabi J.B., Rosen B.P. 1990; Differential mRNA stability controls relative gene expression within the plasmid-encoded arsenical resistance operon.. J Bacteriol 172:2367–2371
    [Google Scholar]
  37. Rosen B.P., Weigel U., Karkaria C., Gangola P. 1988; Molecular characterization of an anion pump. The arsA gene product is an arsenite (antimonate)-stimulated ATPase.. J Biol Chem 263:3067–3070
    [Google Scholar]
  38. Rosenstein R., Peschel P., Wieland B., Gotz F. 1992; Expression and regulation of the Staphylococcus xylosus anti- monite, arsenite, and arsenate resistance operon.. J Bacteriol 174:3676–3683
    [Google Scholar]
  39. Sambrook J., Fritsch E.F., Maniatis T. 1989 MolecularCloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  40. San Francisco M.J.D., Hope C.L., Owolabi J.B., Tisa L.S., Rosen B.P. 1990; Identification of the metalloregulatory element of the plasmid-encoded arsenical resistance operon.. Nucleic Acids Res 18:619–624
    [Google Scholar]
  41. Silver S. 1996; Bacterial resistances to toxic metal ions - a review.. Gene 179:9–19
    [Google Scholar]
  42. Silver S., Ji G., Bröer S., Dey S., Dou D., Rosen B.P. 1993; Orphan enzyme or patriarch of a new tribe: the arsenic resistance ATPase of bacterial plasmids.. Mol Microbiol 8:637–642
    [Google Scholar]
  43. 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
    [Google Scholar]
  44. Takeya K., Amako K. 1966; A rod-shaped Pseudomonas phage.. Virology 28:163–165
    [Google Scholar]
  45. Tisa L.S., Rosen B.P. 1990; Molecular characterization of an anion pump. The ArsB protein is the membrane anchor for the ArsA protein.. J Biol Chem 265:190–194
    [Google Scholar]
  46. Turner R.J., Hou Y., Weiner J.H., Taylor D.E. 1992; The arsenic ATPase efflux pump mediates tellurite resistance.. J Bacteriol 174:3092–3094
    [Google Scholar]
  47. Vieira J., Messing J. 1987; Production of single-stranded plasmid DNA.. Methods Enzymol 153:3–11
    [Google Scholar]
  48. Wang Z., Rossman T.G. 1993; Stable and inducible arsenite resistance in Chinese hamster cells.. Toxicol Appl Pharmacol 118:80–86
    [Google Scholar]
  49. Wang Z., Hou G., Rossman T.G. 1994; Induction of arsenite tolerance and thermotolerance by arsenite occurs by different mechanisms.. Environ Health Perspect 102: (Suppl. 3) 97–100
    [Google Scholar]
  50. Wang Z., Dey S., Rosen B.P., Rossman T.G. 1996; Efflux- mediated resistance to arsenicals in arsenic-resistant and -hypersensitive Chinese hamster cells.. Toxicol Appl Pharmacol 137:112–119
    [Google Scholar]
  51. West S.E.H., Iglewski B.H. 1988; Codon usage in Pseudomonas aeruginosa. . Nucleic Acids Res 16:9323–9335
    [Google Scholar]
  52. Wu J., Rosen B.P. 1991; The ArsR protein is a trans-acting regulatory protein.. Mol Microbiol 5:1331–1336
    [Google Scholar]
  53. Wu J., Rosen B.P. 1993a; Metalloregulated expression of the ars operon.. J Biol Chem 268:52–58
    [Google Scholar]
  54. Wu J., Rosen B.P. 1993b; The arsD gene encodes a second trans-acting regulatory protein of the plasmid-encoded arsenical resistance operon.. Mol Microbiol 8:615–623
    [Google Scholar]
  55. Wu J., Tisa L.S., Rosen B.P. 1992; Membrane topology of the ArsB protein, the membrane subunit of an anion-translocating ATPase.. J Biol Chem 267:12570–12576
    [Google Scholar]
  56. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors.. Gene 33:103–109
    [Google Scholar]
/content/journal/micro/10.1099/00221287-144-10-2705
Loading
/content/journal/micro/10.1099/00221287-144-10-2705
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