1887

Abstract

The Sca permease in the oral bacterium is a member of a family of ATP-binding cassette (ABC)-type transporters for manganese (Mn) and related cations that are associated with streptococcal virulence in a number of infection models. Since Mn has a protective function against oxidative damage in a variety of bacteria, we have investigated the role of Sca permease in oxidative stress tolerance in . A single Mn-dependent superoxide dismutase (SOD), encoded by , is expressed by and was >10-fold up-regulated under oxidative stress conditions. Inactivation of resulted in increased susceptibility of cells to growth inhibition by dioxygen (O), and to killing by paraquat (a superoxide anion generator) and by hydrogen peroxide (HO). Expression of thiol peroxidase, encoded by the gene located immediately downstream of the operon, was also up-regulated under oxidative conditions. Inactivation of led to increased susceptibility of cells to HO, but not to O or paraquat. In low-Mn medium (001 μM Mn) and genes were transcriptionally down-regulated, SOD activity was reduced and cells were more sensitive to growth inhibition by O. A Sca permease-deficient () mutant showed further reduced SOD activity and hypersensitivity to O in medium containing <01 μM Mn. These results demonstrate that the Sca (Mn) permease in is essential for protection against oxidative stress.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-10-3255
2002-10-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/10/1483255a.html?itemId=/content/journal/micro/10.1099/00221287-148-10-3255&mimeType=html&fmt=ahah

References

  1. Archibald, F. S. & Fridovich, I. ( 1981; ). Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J Bacteriol 146, 928-936.
    [Google Scholar]
  2. Auzat, I., Chapuy-Regaud, S., Le Bras, G., Santos, D. D., Ogunniyi, A. D., Le Thomas, I., Garel, J.-R., Paton, J. C. & Trombe, M.-C. ( 1999; ). The NADH oxidase of Streptococcus pneumoniae: its involvement in competence and virulence. Mol Microbiol 34, 1018-1028.[CrossRef]
    [Google Scholar]
  3. Barnard, J. P. & Stinson, M. W. ( 1996; ). The alpha-hemolysin of Streptococcus gordonii is hydrogen peroxide. Infect Immun 64, 3853-3857.
    [Google Scholar]
  4. Beauchamp, C. & Fridovich, I. ( 1971; ). Superoxide dismutase: improved assays and an assay applicable to polyacrylamide gels. Anal Biochem 44, 276-287.[CrossRef]
    [Google Scholar]
  5. Berry, A. M. & Paton, J. C. ( 1996; ). Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun 64, 5255-5262.
    [Google Scholar]
  6. 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]
  7. Burnette-Curley, D., Wells, V., Viscount, H., Munro, C. L., Fenno, J. C., Fives-Taylor, P. & Macrina, F. L. ( 1995; ). FimA, a major virulence factor associated with Streptococcus parasanguis endocarditis. Infect Immun 63, 4669-4674.
    [Google Scholar]
  8. Chang, S. K. & Hassan, H. M. ( 1997; ). Characterization of superoxide dismutase in Streptococcus thermophilus. Appl Environ Microbiol 63, 3732-3735.
    [Google Scholar]
  9. Church, G. M. & Gilbert, W. ( 1984; ). Genomic sequencing. Proc Natl Acad Sci USA 81, 1991-1995.[CrossRef]
    [Google Scholar]
  10. Davies, B. J. ( 1964; ). Disc electrophoresis-II. Method and application to human serum proteins. Ann NY Acad Sci 121, 404-427.
    [Google Scholar]
  11. Demuth, D. R., Duan, Y., Brooks, W., Holmes, A. R., McNab, R. & Jenkinson, H. F. ( 1996; ). Tandem genes encode cell-surface polypeptides SspA and SspB which mediate adhesion of the oral bacterium Streptococcus gordonii to human and bacterial receptors. Mol Microbiol 20, 403-413.[CrossRef]
    [Google Scholar]
  12. DiGuiseppi, J. & Fridovich, I. ( 1982; ). Oxygen toxicity in Streptococcus sanguis. J Biol Chem 257, 4046-4051.
    [Google Scholar]
  13. Dintilhac, A. & Claverys, J. P. ( 1997; ). The adc locus, which affects competence for genetic transformation in Streptococcus pneumoniae, encodes an ABC transporter with a putative lipoprotein homologous to a family of streptococcal adhesins. Res Microbiol 148, 119-131.[CrossRef]
    [Google Scholar]
  14. Douglas, C. W., Heath, J., Hampton, K. K. & Preston, F. E. ( 1993; ). Identity of viridans streptococci isolated from cases of infective endocarditis. J Med Microbiol 39, 179-182.[CrossRef]
    [Google Scholar]
  15. Fenno, J. C., Shaikh, A., Spatafora, G. & Fives-Taylor, P. ( 1995; ). The fimA locus of Streptococcus parasanguis encodes an ATP-binding membrane transport system. Mol Microbiol 15, 849-863.[CrossRef]
    [Google Scholar]
  16. Gerlach, D., Reichardt, W. & Vettermann, S. ( 1998; ). Extracellular superoxide dismutase from Streptococcus pyogenes type 12 strain is manganese-dependent. FEMS Microbiol Lett 160, 217-224.[CrossRef]
    [Google Scholar]
  17. Gibson, C. M. & Caparon, M. G. ( 1996; ). Insertional inactivation of Streptococcus pyogenes sod suggests that prtF is regulated in response to a superoxide signal. J Bacteriol 178, 4688-4695.
    [Google Scholar]
  18. Haisman, R. J. & Jenkinson, H. F. ( 1991; ). Mutants of Streptococcus gordonii Challis over-producing glucosyltransferase. J Gen Microbiol 137, 483-489.[CrossRef]
    [Google Scholar]
  19. Herbig, A. F. & Helmann, J. D. ( 2001; ). Roles of metal ions and hydrogen peroxide in modulating the interaction of the Bacillus subtilis PerR peroxide regulon repressor with operator DNA. Mol Microbiol 41, 849-859.
    [Google Scholar]
  20. Horsburgh, M. J., Clements, M. O., Crossley, H., Ingham, E. & Foster, S. J. ( 2001; ). PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect Immun 69, 3744-3754.[CrossRef]
    [Google Scholar]
  21. Jakubovics, N. S. & Jenkinson, H. F. ( 2001; ). Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147, 1709-1718.
    [Google Scholar]
  22. Jakubovics, N. S., Smith, A. W. & Jenkinson, H. F. ( 2000; ). Expression of the virulence-related Sca (Mn2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol Microbiol 38, 140-153.[CrossRef]
    [Google Scholar]
  23. Jenkinson, H. F. ( 1987; ). Novobiocin-resistant mutants of Streptococcus sanguis with reduced cell hydrophobicity and defective in coaggregation. J Gen Microbiol 133, 1909-1918.
    [Google Scholar]
  24. Jenkinson, H. F., Baker, R. A. & Tannock, G. W. ( 1996; ). A binding-lipoprotein-dependent oligopeptide transport system in Streptococcus gordonii essential for uptake of hexa- and heptapeptides. J Bacteriol 178, 68-77.
    [Google Scholar]
  25. King, K. Y., Horenstein, J. A. & Caparon, M. G. ( 2000; ). Aerotolerance and peroxide resistance in peroxidase and PerR mutants of Streptococcus pyogenes. J Bacteriol 182, 5290-5299.[CrossRef]
    [Google Scholar]
  26. Kitten, T., Munro, C. L., Michalek, S. M. & Macrina, F. L. ( 2000; ). Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect Immun 68, 4441-4451.[CrossRef]
    [Google Scholar]
  27. Kolenbrander, P. E., Andersen, R. N., Baker, R. A. & Jenkinson, H. F. ( 1998; ). The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol 180, 290-295.
    [Google Scholar]
  28. Kolenbrander, P. E., Andersen, R. N. & Ganeshkumar, N. ( 1994; ). Nucleotide-sequence of the Streptococcus gordonii PK488 coaggregation adhesin gene, scaA, and ATP-binding cassette. Infect Immun 62, 4469-4480.
    [Google Scholar]
  29. Krachler, M., Rossipal, E. & Micetic-Turk, D. ( 1999; ). Concentrations of trace elements in sera of newborns, young infants, and adults. Biol Trace Elem Res 68, 121-135.[CrossRef]
    [Google Scholar]
  30. Macrina, F. L., Evans, R. P., Tobian, J. A., Hartley, D. L., Clewell, D. B. & Jones, K. R. ( 1983; ). Novel shuttle plasmid vehicles for EscherichiaStreptococcus transgeneric cloning. Gene 25, 145-150.[CrossRef]
    [Google Scholar]
  31. McCord, J. M. & Fridovich, I. ( 1969; ). Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244, 6049-6055.
    [Google Scholar]
  32. Miller, R. A. & Britigan, B. E. ( 1997; ). Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10, 1-18.
    [Google Scholar]
  33. Nakayama, K. ( 1992; ). Nucleotide sequence of Streptococcus mutans superoxide dismutase gene and isolation of insertion mutants. J Bacteriol 174, 4928-4934.
    [Google Scholar]
  34. Niven, D. F., Ekins, A. & Al-Samaurai, A. A.-W. ( 1999; ). Effects of iron and manganese availability on growth and production of superoxide dismutase by Streptococcus suis. Can J Microbiol 45, 1027-1032.[CrossRef]
    [Google Scholar]
  35. Pericone, C. D., Overweg, K., Hermans, P. W. & Weiser, J. N. ( 2000; ). Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68, 3990-3997.[CrossRef]
    [Google Scholar]
  36. Poyart, C., Quesne, G., Coulon, S., Berche, P. & Trieu-Cuot, P. ( 1998; ). Identification of streptococci to species level by sequencing the gene encoding the manganese-dependent superoxide dismutase. J Clin Microbiol 36, 41-47.
    [Google Scholar]
  37. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  38. Spatafora, G., Van Hoeven, N., Wagner, K. & Fives-Taylor, P. ( 2002; ). Evidence that ORF3 at the Streptococcus parasanguis fimA locus encodes a thiol-specific antioxidant. Microbiology 148, 755-762.
    [Google Scholar]
  39. Tao, L., LeBlanc, D. J. & Ferretti, J. J. ( 1992; ). Novel streptococcal-integration shuttle vectors for gene cloning and inactivation. Gene 120, 105-110.[CrossRef]
    [Google Scholar]
  40. Touati, D. ( 2000; ). Iron and oxidative stress in bacteria. Arch Biochem Biophys 373, 1-6.[CrossRef]
    [Google Scholar]
  41. Tseng, H. J., Srikhanta, Y., McEwan, A. G. & Jennings, M. P. ( 2001; ). Accumulation of manganese in Neisseria gonorrhoeae correlates with resistance to oxidative killing by superoxide anion and is independent of superoxide dismutase activity. Mol Microbiol 40, 1175-1186.[CrossRef]
    [Google Scholar]
  42. Tseng, H. J., McEwan, A. G., Paton, J. C. & Jennings, M. P. ( 2002; ). Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun 70, 1635-1639.[CrossRef]
    [Google Scholar]
  43. Wan, X. Y., Zhou, Y., Yan, Z. Y., Wang, H. L., Hou, Y. D. & Jin, D. Y. ( 1997; ). Scavengase p20: a novel family of bacterial antioxidant enzymes. FEBS Lett 407, 32-36.[CrossRef]
    [Google Scholar]
  44. Whiley, R. A. & Beighton, D. ( 1998; ). Current classification of the oral streptococci. Oral Microbiol Immunol 13, 195-216.[CrossRef]
    [Google Scholar]
  45. Yesilkaya, H., Kadioglu, A., Gingles, N., Alexander, J. E., Mitchell, T. J. & Andrew, P. W. ( 2000; ). Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect Immun 68, 2819-2826.[CrossRef]
    [Google Scholar]
  46. Zhou, Y., Wan, X. Y., Wang, H. L., Yan, Z. Y., Hou, Y. D. & Jin, D. Y. ( 1997; ). Bacterial scavengase p20 is structurally and functionally related to peroxiredoxins. Biochem Biophys Res Commun 233, 848-852.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-10-3255
Loading
/content/journal/micro/10.1099/00221287-148-10-3255
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