Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Feb;177(4):981–986. doi: 10.1128/jb.177.4.981-986.1995

The ars operon of Escherichia coli confers arsenical and antimonial resistance.

A Carlin 1, W Shi 1, S Dey 1, B P Rosen 1
PMCID: PMC176692  PMID: 7860609

Abstract

The chromosomally encoded arsenical resistance (ars) operon subcloned into a multicopy plasmid was found to confer a moderate level of resistance to arsenite and antimonite in Escherichia coli. When the operon was deleted from the chromosome, the cells exhibited hypersensitivity to arsenite, antimonite, and arsenate. Expression of the ars genes was inducible by arsenite. By Southern hybridization, the operon was found in all strains of E. coli examined but not in Salmonella typhimurium, Pseudomonas aeruginosa, or Bacillus subtilis.

Full Text

The Full Text of this article is available as a PDF (285.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Angov E., Brusilow W. S. Use of lac fusions to measure in vivo regulation of expression of Escherichia coli proton-translocating ATPase (unc) genes. J Bacteriol. 1988 Jan;170(1):459–462. doi: 10.1128/jb.170.1.459-462.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bröer S., Ji G., Bröer A., Silver S. Arsenic efflux governed by the arsenic resistance determinant of Staphylococcus aureus plasmid pI258. J Bacteriol. 1993 Jun;175(11):3480–3485. doi: 10.1128/jb.175.11.3480-3485.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chen C. M., Misra T. K., Silver S., Rosen B. P. Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon. J Biol Chem. 1986 Nov 15;261(32):15030–15038. [PubMed] [Google Scholar]
  4. Chen C. M., Mobley H. L., Rosen B. P. Separate resistances to arsenate and arsenite (antimonate) encoded by the arsenical resistance operon of R factor R773. J Bacteriol. 1985 Feb;161(2):758–763. doi: 10.1128/jb.161.2.758-763.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chung C. T., Niemela S. L., Miller R. H. One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2172–2175. doi: 10.1073/pnas.86.7.2172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dey S., Dou D., Rosen B. P. ATP-dependent arsenite transport in everted membrane vesicles of Escherichia coli. J Biol Chem. 1994 Oct 14;269(41):25442–25446. [PubMed] [Google Scholar]
  7. Dey S., Dou D., Tisa L. S., Rosen B. P. Interaction of the catalytic and the membrane subunits of an oxyanion-translocating ATPase. Arch Biochem Biophys. 1994 Jun;311(2):418–424. doi: 10.1006/abbi.1994.1256. [DOI] [PubMed] [Google Scholar]
  8. Dey S., Rosen B. P. Dual mode of energy coupling by the oxyanion-translocating ArsB protein. J Bacteriol. 1995 Jan;177(2):385–389. doi: 10.1128/jb.177.2.385-389.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dou D., Dey S., Rosen B. P. A functional chimeric membrane subunit of an ion-translocating ATPase. Antonie Van Leeuwenhoek. 1994;65(4):359–368. doi: 10.1007/BF00872219. [DOI] [PubMed] [Google Scholar]
  10. Elek S. D., Higney L. Resistogram typing--a new epidemiological tool: application to Escherichia coli. J Med Microbiol. 1970 Feb;3(1):103–110. doi: 10.1099/00222615-3-1-103. [DOI] [PubMed] [Google Scholar]
  11. Gladysheva T. B., Oden K. L., Rosen B. P. Properties of the arsenate reductase of plasmid R773. Biochemistry. 1994 Jun 14;33(23):7288–7293. doi: 10.1021/bi00189a033. [DOI] [PubMed] [Google Scholar]
  12. Hedges R. W., Baumberg S. Resistance to arsenic compounds conferred by a plasmid transmissible between strains of Escherichia coli. J Bacteriol. 1973 Jul;115(1):459–460. doi: 10.1128/jb.115.1.459-460.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hsu C. M., Rosen B. P. Characterization of the catalytic subunit of an anion pump. J Biol Chem. 1989 Oct 15;264(29):17349–17354. [PubMed] [Google Scholar]
  14. Hughes V. M., Datta N. Conjugative plasmids in bacteria of the 'pre-antibiotic' era. Nature. 1983 Apr 21;302(5910):725–726. doi: 10.1038/302725a0. [DOI] [PubMed] [Google Scholar]
  15. Ji G., Silver S. Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9474–9478. doi: 10.1073/pnas.89.20.9474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ji G., Silver S. Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J Bacteriol. 1992 Jun;174(11):3684–3694. doi: 10.1128/jb.174.11.3684-3694.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kaur P., Rosen B. P. Plasmid-encoded resistance to arsenic and antimony. Plasmid. 1992 Jan;27(1):29–40. doi: 10.1016/0147-619x(92)90004-t. [DOI] [PubMed] [Google Scholar]
  18. Kulakauskas S., Wikström P. M., Berg D. E. Efficient introduction of cloned mutant alleles into the Escherichia coli chromosome. J Bacteriol. 1991 Apr;173(8):2633–2638. doi: 10.1128/jb.173.8.2633-2638.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  20. Manoil C., Beckwith J. TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129–8133. doi: 10.1073/pnas.82.23.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Martinez E., Bartolomé B., de la Cruz F. pACYC184-derived cloning vectors containing the multiple cloning site and lacZ alpha reporter gene of pUC8/9 and pUC18/19 plasmids. Gene. 1988 Aug 15;68(1):159–162. doi: 10.1016/0378-1119(88)90608-7. [DOI] [PubMed] [Google Scholar]
  22. Mobley H. L., Rosen B. P. Energetics of plasmid-mediated arsenate resistance in Escherichia coli. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6119–6122. doi: 10.1073/pnas.79.20.6119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mobley H. L., Silver S., Porter F. D., Rosen B. P. Homology among arsenate resistance determinants of R factors in Escherichia coli. Antimicrob Agents Chemother. 1984 Feb;25(2):157–161. doi: 10.1128/aac.25.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Novick R. P., Roth C. Plasmid-linked resistance to inorganic salts in Staphylococcus aureus. J Bacteriol. 1968 Apr;95(4):1335–1342. doi: 10.1128/jb.95.4.1335-1342.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oden K. L., Gladysheva T. B., Rosen B. P. Arsenate reduction mediated by the plasmid-encoded ArsC protein is coupled to glutathione. Mol Microbiol. 1994 Apr;12(2):301–306. doi: 10.1111/j.1365-2958.1994.tb01018.x. [DOI] [PubMed] [Google Scholar]
  26. Owolabi J. B., Rosen B. P. Differential mRNA stability controls relative gene expression within the plasmid-encoded arsenical resistance operon. J Bacteriol. 1990 May;172(5):2367–2371. doi: 10.1128/jb.172.5.2367-2371.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Prentki P., Karch F., Iida S., Meyer J. The plasmid cloning vector pBR325 contains a 482 base-pair-long inverted duplication. Gene. 1981 Sep;14(4):289–299. doi: 10.1016/0378-1119(81)90161-x. [DOI] [PubMed] [Google Scholar]
  28. Rosen B. P., Borbolla M. G. A plasmid-encoded arsenite pump produces arsenite resistance in Escherichia coli. Biochem Biophys Res Commun. 1984 Nov 14;124(3):760–765. doi: 10.1016/0006-291x(84)91023-4. [DOI] [PubMed] [Google Scholar]
  29. Rosenstein R., Nikoleit K., Götz F. Binding of ArsR, the repressor of the Staphylococcus xylosus (pSX267) arsenic resistance operon to a sequence with dyad symmetry within the ars promoter. Mol Gen Genet. 1994 Mar;242(5):566–572. doi: 10.1007/BF00285280. [DOI] [PubMed] [Google Scholar]
  30. Rosenstein R., Peschel A., Wieland B., Götz F. Expression and regulation of the antimonite, arsenite, and arsenate resistance operon of Staphylococcus xylosus plasmid pSX267. J Bacteriol. 1992 Jun;174(11):3676–3683. doi: 10.1128/jb.174.11.3676-3683.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. San Francisco M. J., Hope C. L., Owolabi J. B., Tisa L. S., Rosen B. P. Identification of the metalloregulatory element of the plasmid-encoded arsenical resistance operon. Nucleic Acids Res. 1990 Feb 11;18(3):619–624. doi: 10.1093/nar/18.3.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Silver S., Budd K., Leahy K. M., Shaw W. V., Hammond D., Novick R. P., Willsky G. R., Malamy M. H., Rosenberg H. Inducible plasmid-determined resistance to arsenate, arsenite, and antimony (III) in escherichia coli and Staphylococcus aureus. J Bacteriol. 1981 Jun;146(3):983–996. doi: 10.1128/jb.146.3.983-996.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Silver S., Keach D. Energy-dependent arsenate efflux: the mechanism of plasmid-mediated resistance. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6114–6118. doi: 10.1073/pnas.79.20.6114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith I., Paress P., Cabane K., Dubnau E. Genetics and physiology of the rel system of Bacillus subtilis. Mol Gen Genet. 1980;178(2):271–279. doi: 10.1007/BF00270472. [DOI] [PubMed] [Google Scholar]
  36. Sofia H. J., Burland V., Daniels D. L., Plunkett G., 3rd, Blattner F. R. Analysis of the Escherichia coli genome. V. DNA sequence of the region from 76.0 to 81.5 minutes. Nucleic Acids Res. 1994 Jul 11;22(13):2576–2586. doi: 10.1093/nar/22.13.2576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Summers A. O., Jacoby G. A. Plasmid-determined resistance to boron and chromium compounds in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1978 Apr;13(4):637–640. doi: 10.1128/aac.13.4.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tisa L. S., Rosen B. P. Molecular characterization of an anion pump. The ArsB protein is the membrane anchor for the ArsA protein. J Biol Chem. 1990 Jan 5;265(1):190–194. [PubMed] [Google Scholar]
  39. Tisa L. S., Rosen B. P. Transport systems encoded by bacterial plasmids. J Bioenerg Biomembr. 1990 Aug;22(4):493–507. doi: 10.1007/BF00762959. [DOI] [PubMed] [Google Scholar]
  40. Wu J., Rosen B. P. Metalloregulated expression of the ars operon. J Biol Chem. 1993 Jan 5;268(1):52–58. [PubMed] [Google Scholar]
  41. Wu J., Rosen B. P. The ArsR protein is a trans-acting regulatory protein. Mol Microbiol. 1991 Jun;5(6):1331–1336. doi: 10.1111/j.1365-2958.1991.tb00779.x. [DOI] [PubMed] [Google Scholar]
  42. Wu J., Rosen B. P. The arsD gene encodes a second trans-acting regulatory protein of the plasmid-encoded arsenical resistance operon. Mol Microbiol. 1993 May;8(3):615–623. doi: 10.1111/j.1365-2958.1993.tb01605.x. [DOI] [PubMed] [Google Scholar]
  43. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES