1887

Microbiology Society logo

Volume 149, Issue 5

An inducible tellurite-resistance operon in Free

Abstract

Tellurite resistance (Te) is widespread in nature and it is shown here that the natural resistance of to tellurite is due to a chromosomally located orthologue of plasmid-borne genes found in enteric bacteria. The locus () was identified in a screen of Tn-generated mutants of which one contained an insertion in . The mutant displayed increased susceptibility to tellurite (Te) and complementation with carried on a multicopy plasmid restored high-level Te. Primer extension analysis revealed a single transcriptional start site upstream of , but only with RNA harvested from bacteria grown in the presence of tellurite. Northern blotting and reverse transcriptase-PCR (RT-PCR) analyses confirmed that the operon was inducible by tellurite and to a lesser extent by oxidative stress inducers such as hydrogen peroxide and methyl viologen (paraquat). Direct and inverted repeat sequences were identified in the promoter region as well as motifs upstream of the −35 hexamer that resembled OxyR-binding sequences. Finally, the 390 bp intergenic promoter region located between and showed no DNA sequence identity with any other published sequences, whereas genes exhibited 73–85 % DNA sequence identity. The operon was present in all clinical isolates of and tested and is inferred for and spp. based on screening for high level Te and preliminary PCR analysis. Thus, a chromosomally located inducible tellurite resistance operon appears to be a common feature of the genus .

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): Ter, tellurite resistance
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.25981-0
2003-05-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/5/mic1491285.html?itemId=/content/journal/micro/10.1099/mic.0.25981-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. F., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
     [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. Microbiology 143:1181–1189
     [Google Scholar]
  3. Birnboim H. C., Doly J. 1979; A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523
     [Google Scholar]
  4. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. 1977; Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95–103
     [Google Scholar]
  5. Boltner D., MacMahon C., Pembroke J. T., Strike P., Osborn A. M. 2002; R391: a conjugative integrating mosaic comprised of phage, plasmid and transposon elements. J Bacteriol 184:5158–5169
     [Google Scholar]
  6. De Lorenzo V., Herrero M., Jakkubzik U., Timmis K. N. 1990; Mini-Tn 5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative bacteria. J Bacteriol 172:6568–6572
     [Google Scholar]
  7. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
     [Google Scholar]
  8. Di Tomaso G., Fedi S., Carnevali M., Manegatti M., Taddei C., Zannoni D. 2002; The membrane-bound respiratory chain of Pseudomonas pseudoalcaligenes KF707 cells grown in the presence or absence of potassium tellurite. Microbiology 148:1699–1708
     [Google Scholar]
  9. Fleming A. 1932; On the specific antibacterial properties of penicillin and potassium tellurite. J Pathol Bacteriol 35:831–842
     [Google Scholar]
  10. Garberg P., Engman L., Tolmachev V., Lundqvist H., Gerdes R. G., Cotgreave I. A. 1999; Binding of tellurium to hepatocellular selenoproteins during incubation with inorganic tellurite: consequences for the activity of selenium-dependent glutathione peroxidase. Inter J Biochem Cell Biol 31:291–301
     [Google Scholar]
  11. 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 Genet 241:203–212
     [Google Scholar]
  12. Hofmann K., Stoffel W. 1993; tmbase – A database of membrane spanning protein segments. Biol Chem Hoppe-Seyler 374:166–173
     [Google Scholar]
  13. Hoffman P. S., Falkinham J. O. III 1981; Induction of tryptophanase in short cells and swarm cells of Proteus vulgaris . J Bacteriol 148:736–738
     [Google Scholar]
  14. Hoffman P. S., Butler C. A., Quinn F. D. 1989; Cloning and temperature-dependent expression in Escherichia coli of a Legionella pneumophila gene coding for a genus common 60 kilodalton antigen. Infect Immun 57:1731–1739
     [Google Scholar]
  15. Hoffman P. S., Ripley M., Weeratna R. 1992; Cloning and nucleotide sequence of a gene ( ompS ) encoding the major outer membrane protein of Legionella pneumophila . J Bacteriol 174:914–920
     [Google Scholar]
  16. Hohn B., Collins J. 1980; A small cosmid for efficient cloning of large DNA fragments. Gene 11:291–298
     [Google Scholar]
  17. Hoopes B. C., McClure W. R. 1987; Strategies in regulation of transcription initiation. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp 1231–1240 Edited by Ingraham J. L., Low K. B., Magasanik B., Neidhardt F. C., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  18. Jobling M. G., Ritchie D. A. 1987; Genetic and physical analysis of plasmid genes expressing inducible resistance of tellurite in Escherichia coli . Mol Gen Genet 208:288–293
     [Google Scholar]
  19. Jobling M. G., Ritchie D. A. 1988; The nucleotide sequence of a plasmid determinant for resistance to tellurium anions. Gene 66:245–258
     [Google Scholar]
  20. Kieny M. P., Lathe R., Lecocq J. P. 1983; New versatile cloning and sequencing vectors based on bacteriophage M13. Gene 26:91–99
     [Google Scholar]
  21. Klein P., Kanehisa M., DeLisi C. 1985; The detection and classification of membrane-spanning proteins. Biochim Biophys Acta 815:468–476
     [Google Scholar]
  22. Kormutakova R., Klucar L., Turna J. 2000; DNA sequence analysis of the tellurite-resistance determinant from clinical strain of Escherichia coli and identification of essential genes. BioMetals 13:135–139
     [Google Scholar]
  23. Kouzarides T., Ziff E. 1989; Leucine zipper of fos, jun and GCN4 dictate dimerization specificity and thereby control DNA binding. Nature 340:568–571
     [Google Scholar]
  24. Kroczek R. A., Siebert E. 1990; Optimization of northern blot analysis by vacuum-blotting, RNA transfer, and ultraviolet fixation. Anal Biochem 184:90–95
     [Google Scholar]
  25. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  26. Murata M., Ohnishi T., Ara J. 13 other authors 2002; Complete nucleotide sequence of plasmid Rts1: implications for evolution of large plasmid genomes. J Bacteriol 184:3194–3202
     [Google Scholar]
  27. Nakai K., Kanehisa M. 1991; Expert system for predicting protein localization sites in Gram-negative bacteria. Prot Struct Funct Genet 11:95–110
     [Google Scholar]
  28. Ochsner U. A., Vasil M. L., Alsabbagh E., Parvatiyar K., Hassett D. J. 2000; Role of the Pseudomonas aeruginosa oxyR - regG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB - ankB , ahpB and ahpC- ahpF . J Bacteriol 182:4533–4544
     [Google Scholar]
  29. O'Connell W. A., Hickey E. K., Cianciotto N. P. 1996; A Legionella pneumophila gene that promotes hemin binding. Infect Immun 64:842–848
     [Google Scholar]
  30. Parkhill J., Wren B. W., Thomson N. R. 32 other authors 2001; Genome sequence of Yersinia pestis , the causative agent of plague. Nature 413:523–527
     [Google Scholar]
  31. Pearson W. R. 1990; Rapid and sensitive sequence comparison with fastp and fasta. Methods Enzymol 183:63–98
     [Google Scholar]
  32. Perna N. T., Plunkett G. III, Burland V. 25 other authors 2001; Genome sequence of enterohaemorrhagic Escherichia coli O157 : H7. Nature 409:529–533
     [Google Scholar]
  33. Rahaman M. M., Morshed M. G., Sultanul Aziz K. M., Munshi M. M. 1986; Improved medium for isolating Shigella . Lancet 1:271–272
     [Google Scholar]
  34. 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]
  35. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
     [Google Scholar]
  36. Senior B. W. 1977; The Dienes phenomenon: identification of the determinants of compatibility. J Gen Microbiol 102:235–244
     [Google Scholar]
  37. Shimada T., Sakazaki R., Fujimura S., Niwano K., Mishina M., Takizawa K. 1990; A new selective, differential agar medium for isolation of Vibrio cholerae O1: PMT (polymyxin-mannose-tellurite) agar. Jpn J Med Sci Biol 43:37–41
     [Google Scholar]
  38. Short J. M., Fernandez J. M., Sorge J. A., Huse W. D. 1988; λ ZAP: A bacteriophage λ expression vector with in vivo excision properties. Nucleic Acids Res 16:7583–7590
     [Google Scholar]
  39. Silhavy T. J., Berman M. L., Enquist L. W. 1984 Experiments with Gene Fusions Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  40. Taylor D. E. 1999; Bacterial tellurite resistance. Trends Microbiol 7:111–115
     [Google Scholar]
  41. Taylor D. E., Rooker M., Keelan M., Ng L.-K., Martin I., Perna N. T., Burland N. T. V., Blattner F. R. 2002; Genomic variability of O islands encoding tellurite resistance in enterohemorrhagic Escherichia coli O157 : H7 isolates. J Bacteriol 184:4690–4698
     [Google Scholar]
  42. 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
     [Google Scholar]
  43. Trutko S. M., Akimenko V. K., Suzina N. E., Anisimova L. A., Shlyapnikov M., Baskunov B. P., Duda V. I., Boronin A. M. 2000; Involvement of the respiratory chain of Gram-negative bacteria in the reduction of tellurite. Arch Microbiol 173:178–186
     [Google Scholar]
  44. Turner R. J., Weiner J. H., Taylor D. E. 1999; Tellurite-mediated thiol oxidation in Escherichia coli . Microbiology 145:2549–2557
     [Google Scholar]
  45. Walter E. G., Taylor D. E. 1992; Plasmid-mediated resistance to tellurite: expressed and cryptic. Plasmid 27:52–64
     [Google Scholar]
  46. 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 IncH12 plasmid R478. J Bacteriol 177:5016–5027
     [Google Scholar]
  47. Whelan K. F., Sherburne R. K., Taylor D. E. 1997; Characterisation of a region of the IncH12 plasmid R478 which protects Escherichia coli from toxic effects specified by components of the tellurite, phage and colicin resistance cluster. J Bacteriol 179:63–71
     [Google Scholar]
  48. Zadic P. M., Chapman P. A., Siddons C. A. 1993; Use of tellurite for the selection of verocytotoxigenic Escherichia coli O157. J Med Microbiol 39:155–158
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.25981-0
Loading
An inducible tellurite-resistance operon in Proteus mirabilis
Microbiology 149, 1285 (2003); https://doi.org/10.1099/mic.0.25981-0
/content/journal/micro/10.1099/mic.0.25981-0
/content/journal/micro/10.1099/mic.0.25981-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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