1887

Abstract

The oxyanion of tellurium, tellurite (), is toxic to most micro-organisms, particularly Gram-negative bacteria. The mechanism of tellurite toxicity is presently unknown. Many heavy metals and oxyanions, including tellurite, interact with reduced thiols (RSH). To determine if tellurite interaction with RSH groups is involved in the toxicity mechanism, the RSH content of cultures was assayed. After exposure to tellurite, cells were harvested and lysed in the presence of the RSH-specific reagent 5,5’-dithiobis(2-nitrobenzoic acid). Upon exposure of tellurite-susceptible cells to , the RSH content decreased markedly. Resistance to potassium tellurite (Te) in Gram-negative bacteria is encoded by plasmids of incompatibility groups IncFI, IncPα, IncHI2, IncHI3 and IncHII, as well as the operon from the chromosome. When cells harbouring a Te determinant were exposed to , only a small fraction of the RSH content became oxidized. In addition to tellurite-dependent thiol oxidation, the resistance of mutants affected in proteins involved in disulfide-bond formation () was investigated. Mutant strains of and were found to be hypersensitive to tellurite (MIC 0008–0015 μg KTeO ml compared to wild-type with MICs of 1–2 μg KTeO ml). In contrast, and mutants showed no hypersensitivity. The results suggest that hypersensitivity to tellurite is reliant on the presence of an isomerase activity and not the thiol oxidase activity of the Dsb proteins. The results establish that the Te determinants play an important role in maintaining homeostasis of the intracellular reducing environment within Gram-negative cells through specific reactions with either or thiol:tellurium products.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-145-9-2549
1999-09-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/145/9/1452549a.html?itemId=/content/journal/micro/10.1099/00221287-145-9-2549&mimeType=html&fmt=ahah

References

  1. Albeck A. H. W., Sredni B., Albeck M.. 1998; Tellurium compounds: selective inhibition of cysteine proteases and model reaction with thiols. Inorg Chem37:1704–1712[CrossRef]
    [Google Scholar]
  2. Avazeri C., Turner R. J., Pommier J., Weiner J. H., Giordano G., Vermeglio A.. 1997; Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite. Microbiology143:1181–1189[CrossRef]
    [Google Scholar]
  3. Bachmann B. J.. 1972; Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev36:525–557
    [Google Scholar]
  4. Bardwell J. C. A., McGovern K., Beckwith J.. 1991; Identification of a protein required for disulfide bond formation in vivo. Cell67:681–589
    [Google Scholar]
  5. Boyer H. W., Roulland-Dussoix D.. 1969; A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol41:459–472[CrossRef]
    [Google Scholar]
  6. Bradley D. E.. 1985; Detection of tellurite-resistance determinants in IncP plasmids. J Gen Microbiol131:3135–3137
    [Google Scholar]
  7. Bradley D. E., Hughes V. M., Richards H., Datta N.. 1982; R plasmids of a new incompatibility group determine constitutive production of H pili. Plasmid7:230–238[CrossRef]
    [Google Scholar]
  8. Chiong M., Gonzalez E., Barra R., Vasquez C.. 1988; Purification and biochemical characterization of tellurite-reducing activities from Thermus thermophilus HB8. J Bacteriol170:3269–3273
    [Google Scholar]
  9. Cournoyer B., Watanabe S., Vivian A.. 1998; A tellurite-resistance genetic determinant from phytopathogenic pseudomonads encodes a thiopurine methyltransferase: evidence of a widely-conserved family of methyltransferases. Biochim Biophys Acta1397:161–168[CrossRef]
    [Google Scholar]
  10. Datta N., Hughes V. M.. 1983; Plasmids of the same Inc groups in Enterobacteria before and after the medical use of antibiotics. Nature306:616–617[CrossRef]
    [Google Scholar]
  11. Deuticke B., Lutkemeier P., Poser B.. 1992; Tellurite-induced damage of the erythrocyte membrane. Manifestations and mechanisms. Biochim Biophys Acta1109:97–107[CrossRef]
    [Google Scholar]
  12. Guilhot C., Jander G., Martin N. L., Beckwith J.. 1995; Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc Natl Acad Sci USA92:9895–9899[CrossRef]
    [Google Scholar]
  13. Hill S. M., Jobling M. G., Lloyd B. H., Strike P., Ritchie D. A.. 1993; Functional expression of the tellurite resistance determinant from the IncHI-2 plasmid pMER610. Mol Gen Genet241:203–212
    [Google Scholar]
  14. Jander G., Martin N. L., Beckwith J.. 1994; Two cysteines in each periplasmic domain of the membrane protein DsbB are required for its function in protein disulfide bond formation. EMBO J13:5121–5127
    [Google Scholar]
  15. Jobling M. G., Ritchie D. A.. 1987; Genetic and physical analysis of plasmid genes expressing inducible resistance to tellurite in Escherichia coli. Mol Gen Genet208:288–293[CrossRef]
    [Google Scholar]
  16. Jobling M. G., Ritchie D. A.. 1988; The nucleotide sequence of a plasmid determinant for resistance to tellurium anions. Gene66:245–258[CrossRef]
    [Google Scholar]
  17. Keane D.. 1990; A genetic study of the HII incompatibility group plasmid pHH1457-2 MSc thesis University College; Galway Ireland:
    [Google Scholar]
  18. Kishigami S., Kanaya E., Kikuchi M., Ito K.. 1995; DsbA-DsbB interaction through their active site cysteines. J Biol Chem270:17072–17074[CrossRef]
    [Google Scholar]
  19. Liangyau Y., Kangming H., Duanren C., Cangmin Y., Zheng O.. 1993; Evidence for telluroamino acid in biological materials and some rules of assimilation of inorganic tellurium by yeast. Anal Biochem209:318–322[CrossRef]
    [Google Scholar]
  20. Lloyd-Jones G., Osborne M., Ritchie D. A., Strike P., Hobman J. L., Brown N. L., Rouch D. A.. 1994; Accumulation and intracellular fate of tellurite in tellurite-resistant Escherichia coli: a model for the mechanism of resistance. FEMS Microbiol Lett118:113–120[CrossRef]
    [Google Scholar]
  21. Lundblad R. L.. 1958; Techniques in Protein Modification Boca Raton FL: CRC Press;
    [Google Scholar]
  22. Markwell M. A. K., Haas S. M., Bieber L. L., Tolbert N. E.. 1978; A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem87:206–210[CrossRef]
    [Google Scholar]
  23. Means G. E., Feeney R. E.. 1971; Chemical Modification of Proteins San Francisco: Holden-Day Inc;
    [Google Scholar]
  24. Missiakas D., Raina S.. 1997; Protein folding in the bacterial periplasm. J Bacteriol179:2465–2471
    [Google Scholar]
  25. Moore M. D., Kaplan S.. 1992; Identification of intrinsic high-level resistance to rare-earth oxides and oxyanions in members of the class Proteobacteria: characterization of tellurite, selenite, and rhodium sesquioxide reduction in Rhodobacter sphaeroides. J Bacteriol174:1505–1514
    [Google Scholar]
  26. Moscoso H., Saavedra C., Loyola C., Pichuantes S., Vásquez C.. 1998; Biochemical characterization of tellurite-reducing activities of Bacillus stearothermophilus V. Res Microbiol149:389–397[CrossRef]
    [Google Scholar]
  27. O’Gara J. P., Gomelsky M., Kaplan S.. 1997; Identification and molecular genetic analysis of multiple loci contributing to high-level tellurite resistance in Rhodobacter sphaeroides 2.4.1. Appl Environ Microbiol63:4713–4720
    [Google Scholar]
  28. Rensing C., Mitra B., Rosen B. P.. 1997; Insertional inactivation of dsbA produces sensitivity to cadmium and zinc in Escherichia coli. J Bacteriol179:2769–2771
    [Google Scholar]
  29. Rietsch A. D. B., Martin N., Beckwith J.. 1996; An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proc. Natl Acad Sci USA93:13048–13053[CrossRef]
    [Google Scholar]
  30. Roussel A. F., Chabbert Y. A.. 1978; Taxonomy and epidemiology of gram-negative bacterial plasmids studied by DNA-DNA hybridization in formamide. J Gen Microbiol104:269–276[CrossRef]
    [Google Scholar]
  31. Stafford S. J., Humphres D. P., Lund P. A.. 1999; Mutations in dsbA and dsbB, but not dsbC, lead to an enhanced sensitivity of Escherichia coli to Hg2+ and Cd2+. FEMS Microbiol Lett174:179–184[CrossRef]
    [Google Scholar]
  32. Strack B., Lessl M., Calendar R., Lanka E.. 1992; Sequence motif, -E-G-Y-A-T-A-, identified within the primase domains of plasmid-encoded I- and P-type DNA primases and the α protein of the Escherichia coli satellite phage P4. J Biol Chem267:13062–13072
    [Google Scholar]
  33. Summers A. O., Jacoby G. A.. 1977; Plasmid-determined resistance to tellurium compounds. J Bacteriol129:276–281
    [Google Scholar]
  34. Taylor D. E.. 1999; Bacterial tellurite resistance. Trends Microbiol7:111–115[CrossRef]
    [Google Scholar]
  35. Taylor D. E., Bradley D. E.. 1987; Location on RP4 of a tellurite resistance determinant not normally expressed in IncP α plasmids. Antimicrob Agents Chemother31:823–825[CrossRef]
    [Google Scholar]
  36. Taylor D. E., Levine J. G.. 1980; Studies of temperature-sensitive transfer and maintenance of H incompatibility group plasmids. J Gen Microbiol116:475–484
    [Google Scholar]
  37. Taylor D. E., Summers A. O.. 1979; Association of tellurium resistance and bacteriophage inhibition confered by R plasmids. J Bacteriol139:1430–1433
    [Google Scholar]
  38. Taylor D. E., Walter E. G., Sherburne R., Bazett-Jones D. P.. 1988; Structure and location of tellurium deposited in Escherichia coli cells harboring tellurite resistance plasmids. J. Ultrastruct Mol Struct Res99:18–26[CrossRef]
    [Google Scholar]
  39. Taylor D. E., Hou Y., Turner R. J., Weiner J. H.. 1994; Location of a potassium tellurite resistance operon (tehAtehB) within the terminus of Escherichia coli K-12. J Bacteriol176:2740–2742
    [Google Scholar]
  40. Terai T., Kamahara T., Yamamura Y.. 1958; Tellurite reductase from Mycobacterium avium. J Bacteriol75:535–539
    [Google Scholar]
  41. Thomas C. M., Meyer R., Helinski D. R.. 1980; Regions of broad-host-range plasmid RK2 which are essential for replication and maintenance. J Bacteriol141:213–222
    [Google Scholar]
  42. Trutko S. M., Suzina N. E., Duda V. I., Akimenko V. K., Boronin A. M.. 1998; Involvement of the respiratory chain in potassium tellurite reduction in bacteria. Dokl Biochem358:13–15
    [Google Scholar]
  43. Turner R. J., Hou Y., Weiner J. H., Taylor D. E.. 1992; The arsenical ATPase efflux pump mediates tellurite resistance. J Bacteriol174:3092–3094
    [Google Scholar]
  44. Turner R. J., Weiner J. H., Taylor D. E.. 1994a; In vivo complementation and site-specific mutagenesis of the tellurite resistance determinant kilAtelAB from IncP α plasmid RK2Ter. Microbiology140:1319–1326[CrossRef]
    [Google Scholar]
  45. Turner R. J., Weiner J. H., Taylor D. E.. 1994b; Characterization of the growth inhibition phenotype of the kilAtelAB operon from IncP α plasmid RK2Ter. Biochem Cell Biol72:333–342[CrossRef]
    [Google Scholar]
  46. Turner R. J., Weiner J. H., Taylor D. E.. 1995a; Neither reduced uptake nor increased efflux is encoded by tellurite resistance determinants expressed in Escherichia coli. Can J Microbiol41:92–98[CrossRef]
    [Google Scholar]
  47. Turner R. J., Weiner J. H., Taylor D. E.. 1995b; The tellurite-resistance determinants tehAtehB and klaAklaBtelB have different biochemical requirements. Microbiology141:3133–3140[CrossRef]
    [Google Scholar]
  48. Turner R. J., Taylor D. E., Weiner J. H.. 1997; Expression of Escherichia coli TehA gives resistance to antiseptics and disinfectants similar to that conferred by multidrug resistance efflux pumps. Antimicrob Agents Chemother41:440–444
    [Google Scholar]
  49. Walter E. G., Taylor D. E.. 1989; Comparison of tellurite resistance determinants from the IncP α plasmid RP4Ter and the IncHII plasmid pHH1508a. J Bacteriol171:2160–2165
    [Google Scholar]
  50. Walter E. G., Thomas C. M., Ibbotson J. P., Taylor D. E.. 1991a; Transcriptional analysis, translational analysis, and sequence of the kilA-tellurite resistance region of plasmid RK2TeR. J Bacteriol173:1111–1119
    [Google Scholar]
  51. Walter E. G., Weiner J. H., Taylor D. E.. 1991b; Nucleotide sequence and overexpression of the tellurite resistance determinant from the IncHII plasmid pHH1508a. Gene101:1–7[CrossRef]
    [Google Scholar]
  52. Whelan K. F.. 1958; Genetic analysis of the HI2 incompatibility group plasmid R478 PhD thesis University College; Galway Ireland:
    [Google Scholar]
  53. Whelan K. F., Colleran E., Taylor D. E.. 1995; Phage inhibition, colicin resistance, and tellurite resistance are encoded by a single cluster of genes on the IncHI2 plasmid R478. J Bacteriol177:5016–5027
    [Google Scholar]
  54. Whelan K. F., Sherburne R. K., Taylor D. E.. 1997; Characterization of a region of the IncHI2 plasmid R478 which protects Escherichia coli from toxic effects specified by components of tellurite phage and colicin resistance cluster. J Bacteriol178:63–71
    [Google Scholar]
  55. Woolfolk C. A., Whitely H. R.. 1962; Reduction of inorganic compounds with molecular hydrogen by Micrococcus lactilyticus. I. Stoichiometry with compounds of arsenic, selenium, tellurium, transition and other elements. J Bacteriol84:647–658
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-145-9-2549
Loading
/content/journal/micro/10.1099/00221287-145-9-2549
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