1887

Abstract

A putative operon encoding a probable zinc-responsive regulatory element () and components of an ABC-type transporter () have been characterized in . The gene was inactivated but apparently this did not alter Zn uptake. Expression of is at a low level under a range of ion conditions. To allow inducible expression of the operon, a construct was made placing it under the control of the IPTG-inducible P promoter. Using this approach, it was shown that is able to repress expression of the entire operon in a Zn-dependent manner, and that and are likely to be involved in high-affinity ion uptake. has no apparent role in pathogenicity in a lesion model of infection.

Keyword(s): fur , metals , regulation , transcription and zinc
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-5-1259
2001-05-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/5/1471259a.html?itemId=/content/journal/micro/10.1099/00221287-147-5-1259&mimeType=html&fmt=ahah

References

  1. Achenbach, L. A. & Yang, W. ( 1997; ). The fur gene from Klebsiella pneumoniae: characterization, genomic organization and phylogenetic analysis. Gene 185, 201-207.[CrossRef]
    [Google Scholar]
  2. Althaus, E. W., Outten, C. E., Olson, K. E., Cao, H. & O’Halloran, T. V. ( 1999; ). The ferric uptake regulation (Fur) repressor is a zinc metalloprotein. Biochemistry 38, 6559-6569.[CrossRef]
    [Google Scholar]
  3. Bearden, S. W. & Perry, R. D. ( 1999; ). The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32, 403-414.[CrossRef]
    [Google Scholar]
  4. Bsat, N., Herbig, A., Casillas-Martinez, L., Setlow, P. & Helmann, J. D. ( 1998; ). Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol Microbiol 29, 189-198.[CrossRef]
    [Google Scholar]
  5. Chan, P. F. & Foster, S. J. ( 1998; ). The role of environmental factors in the regulation of virulence-determinant expression in Staphylococcus aureus 8325-4. Microbiology 144, 2469-2479.[CrossRef]
    [Google Scholar]
  6. Chan, P. F., Foster, S. J., Ingham, E. & Clements, M. O. ( 1998; ). The Staphylococcus aureus alternative sigma factor sigmaB controls the environmental stress response but not starvation survival or pathogenicity in a mouse abscess model. J Bacteriol 180, 6082-6089.
    [Google Scholar]
  7. Clements, M. O., Watson, S. P. & Foster, S. J. ( 1999; ). Characterization of the major superoxide dismutase of Staphylococcus aureus and its role in starvation survival, stress resistance, and pathogenicity. J Bacteriol 181, 3898-3903.
    [Google Scholar]
  8. Cockayne, A., Hill, P. J., Powell, N. B., Bishop, K., Sims, C. & Williams, P. ( 1998; ). Molecular cloning of a 32-kilodalton lipoprotein component of a novel iron-regulated Staphylococcus epidermidis ABC transporter. Infect Immun 66, 3767-3774.
    [Google Scholar]
  9. Cornelissen, C. N., Kelley, M., Hobbs, M. M., Anderson, J. E., Cannon, J. G., Cohen, M. S. & Sparling, P. F. ( 1998; ). The transferrin receptor expressed by gonococcal strain FA1090 is required for the experimental infection of human male volunteers. Mol Microbiol 27, 611-616.[CrossRef]
    [Google Scholar]
  10. Courcol, R. J., Trivier, D., Bissinger, M. C., Martin, G. R. & Brown, M. R. ( 1997; ). Siderophore production by Staphylococcus aureus and identification of iron-regulated proteins. I nfect Immun 65, 1944-1948.
    [Google Scholar]
  11. Dalet, K., Gouin, E., Cenatiempo, Y., Cossart, P. & Hechard, Y. ( 1999; ). Characterisation of a new operon encoding a Zur-like protein and an associated ABC zinc permease in Listeria monocytogenes. FEMS Microbiol Lett 174, 111-116.[CrossRef]
    [Google Scholar]
  12. Dawson-Saunders, B. & Trapp, R. G. (1990). Basic and Clinical Biostatistics. Norwalk, CT: Appleton & Lange.
  13. Dintilhac, A., Alloing, G., Granadel, C. & Claverys, J. P. ( 1997; ). Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol 25, 727-739.[CrossRef]
    [Google Scholar]
  14. Domingue, P. A., Lambert, P. A. & Brown, M. R. ( 1989; ). Iron depletion alters surface-associated properties of Staphylococcus aureus and its association to human neutrophils in chemiluminescence. FEMS Microbiol Lett 50, 265-268.
    [Google Scholar]
  15. Driessen, C., Hirv, K., Kirchner, H. & Rink, L. ( 1995a; ). Divergent effects of zinc on different bacterial pathogenic agents. J Infect Dis 171, 486-489.[CrossRef]
    [Google Scholar]
  16. Driessen, C., Hirv, K., Kirchner, H. & Rink, L. ( 1995b; ). Zinc regulates cytokine induction by superantigens and lipopolysaccharide. Immunology 84, 272-277.
    [Google Scholar]
  17. Escolar, L., Perez-Martin, J. & de Lorenzo, V. ( 1999; ). Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181, 6223-6229.
    [Google Scholar]
  18. Foster, S. J. ( 1991; ). Cloning, expression, sequence analysis and biochemical characterization of an autolytic amidase of Bacillus subtilis 168 trpC2. J Gen Microbiol 137, 1987-1998.[CrossRef]
    [Google Scholar]
  19. Gaballa, A. & Helmann, J. D. ( 1998; ). Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180, 5815-5821.
    [Google Scholar]
  20. Guerout-Fleury, A. M., Shazand, K., Frandsen, N. & Stragier, P. ( 1995; ). Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167, 335-336.[CrossRef]
    [Google Scholar]
  21. Haag, H., Fiedler, H. P., Meiwes, J., Drechsel, H., Jung, G. & Zahner, H. ( 1994; ). Isolation and biological characterization of staphyloferrin B, a compound with siderophore activity from staphylococci. FEMS Microbiol Lett 115, 125-130.[CrossRef]
    [Google Scholar]
  22. Heidrich, C., Hantke, K., Bierbaum, G. & Sahl, H. G. ( 1996; ). Identification and analysis of a gene encoding a Fur-like protein of Staphylococcus epidermidis. FEMS Microbiol Lett 140, 253-259.[CrossRef]
    [Google Scholar]
  23. Heinrichs, J. H., Gatlin, L. E., Kunsch, C., Choi, G. H. & Hanson, M. S. ( 1999; ). Identification and characterization of SirA, an iron-regulated protein from Staphylococcus aureus. J Bacteriol 181, 1436-1443.
    [Google Scholar]
  24. Horsburgh, M. J., Ingham, E. & Foster, S. J. ( 2001; ). In Staphylococcus aureus, Fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol 183, 468-475.[CrossRef]
    [Google Scholar]
  25. Janakiraman, A. & Slauch, J. M. ( 2000; ). The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol Microbiol 35, 1146-1155.[CrossRef]
    [Google Scholar]
  26. Janulczyk, R., Pallon, J. & Bjorck, L. ( 1999; ). Identification and characterization of a Streptococcus pyogenes ABC transporter with multiple specificity for metal cations. Mol Microbiol 34, 596-606.[CrossRef]
    [Google Scholar]
  27. Kreiswirth, B. N., Lofdahl, S., Betley, M. J., O’Reilly, M., Schlievert, P. M., Bergdoll, M. S. & Novick, R. P. ( 1983; ). The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305, 709-712.[CrossRef]
    [Google Scholar]
  28. Levin, J. D., Shapiro, R. & Demple, B. ( 1991; ). Metalloenzymes in DNA repair. Escherichia coli endonuclease IV and Saccharomyces cerevisiae Apn1. J Biol Chem 266, 22893-22898.
    [Google Scholar]
  29. Lewis, D. A., Klesney-Tait, J., Lumbley, S. R., Ward, C. K., Latimer, J. L., Ison, C. A. & Hansen, E. J. ( 1999; ). Identification of the znuA-encoded periplasmic zinc transport protein of Haemophilus ducreyi. Infect Immun 67, 5060-5068.
    [Google Scholar]
  30. Lindsay, J. A. & Riley, T. V. ( 1994; ). Staphylococcal iron requirements, siderophore production, and iron-regulated protein expression. Infect Immun 62, 2309-2314.
    [Google Scholar]
  31. Lindsay, J. A., Riley, T. V. & Mee, B. J. ( 1995; ). Staphylococcus aureus but not Staphylococcus epidermidis can acquire iron from transferrin. Microbiology 141, 197-203.[CrossRef]
    [Google Scholar]
  32. Lindsay, J. A., Ruzin, A., Ross, H. F., Kurepina, N. & Novick, R. P. ( 1998; ). The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29, 527-543.[CrossRef]
    [Google Scholar]
  33. Litwin, C. M. & Calderwood, S. B. ( 1993; ). Role of iron in regulation of virulence genes. Clin Microbiol Rev 6, 137-149.
    [Google Scholar]
  34. Magneson, G. R., Puvathingal, J. M. & Ray, W. J.Jr ( 1987; ). The concentrations of free Mg2+ and free Zn2+ in equine blood plasma. J Biol Chem 262, 11140-11148.
    [Google Scholar]
  35. Meiwes, J., Fiedler, H. P., Haag, H., Zahner, H., Konetschny-Rapp, S. & Jung, G. ( 1990; ). Isolation and characterization of staphyloferrin A, a compound with siderophore activity from Staphylococcus hyicus DSM 20459. FEMS Microbiol Lett 55, 201-205.
    [Google Scholar]
  36. Modun, B. & Williams, P. ( 1999; ). The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect Immun 67, 1086-1092.
    [Google Scholar]
  37. Modun, B., Kendall, D. & Williams, P. ( 1994; ). Staphylococci express a receptor for human transferrin: identification of a 42-kilodalton cell wall transferrin-binding protein. Infect Immun 62, 3850-3858.
    [Google Scholar]
  38. Modun, B., Evans, R. W., Joannou, C. L. & Williams, P. ( 1998; ). Receptor-mediated recognition and uptake of iron from human transferrin by Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 66, 3591-3596.
    [Google Scholar]
  39. Novak, R., Braun, J. S., Charpentier, E. & Tuomanen, E. ( 1998; ). Penicillin tolerance genes of Streptococcus pneumoniae: the ABC-type manganese permease complex Psa. Mol Microbiol 29, 1285-1296.[CrossRef]
    [Google Scholar]
  40. Novick, R. ( 1967; ). Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33, 155-166.[CrossRef]
    [Google Scholar]
  41. Novick, R. P. ( 1991; ). Genetic systems in staphylococci. Methods Enzymol 204, 587-636.
    [Google Scholar]
  42. Patzer, S. I. & Hantke, K. ( 1998; ). The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28, 1199-1210.[CrossRef]
    [Google Scholar]
  43. Que, Q. & Helmann, J. D. ( 2000; ). Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins. Mol Microbiol 35, 1454-1468.
    [Google Scholar]
  44. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  45. Schenk, S. & Laddaga, R. A. ( 1992; ). Improved method for electroporation of Staphylococcus aureus. FEMS Microbiol Lett 73, 133-138.
    [Google Scholar]
  46. Trivier, D., Davril, M., Houdret, N. & Courcol, R. J. ( 1995; ). Influence of iron depletion on growth kinetics, siderophore production, and protein expression of Staphylococcus aureus. FEMS Microbiol Lett 127, 195-199.[CrossRef]
    [Google Scholar]
  47. Vagner, V., Dervyn, E. & Ehrlich, S. D. ( 1998; ). A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144, 3097-3104.[CrossRef]
    [Google Scholar]
  48. Watson, S. P., Clements, M. O. & Foster, S. J. ( 1998; ). Characterization of the starvation-survival response of Staphylococcus aureus. J Bacteriol 180, 1750-1758.
    [Google Scholar]
  49. Xiong, A. & Jayaswal, R. K. ( 1998; ). Molecular characterization of a chromosomal determinant conferring resistance to zinc and cobalt ions in Staphylococcus aureus. J Bacteriol 180, 4024-4029.
    [Google Scholar]
  50. Xiong, A., Singh, V. K., Cabrera, G. & Jayaswal, R. K. ( 2000; ). Molecular characterization of the ferric-uptake regulator, fur, from Staphylococcus aureus. Microbiology 146, 659-668.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-5-1259
Loading
/content/journal/micro/10.1099/00221287-147-5-1259
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