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Abstract

The roles of two adjacent genes in the chromosome with functions in starvation survival and the response to stressful conditions have been characterized. One of these, , encoding a hypoxanthine–guanine phosphoribosyltransferase homologue, was initially identified in a transposon mutagenesis screen. Mutation of affects starvation survival in amino-acid-limiting conditions and the ability of to grow in high-salt concentrations. Downstream of is , which encodes a membrane-bound, ATP- and Zn-dependent ‘AAA’-type protease. Mutation of in leads to pleiotropic defects including slower growth, sensitivity to salt, acid, methyl viologen and potassium tellurite stresses, and reduced survival in amino-acid- or phosphate-limiting conditions. Both and gene fusions are expressed maximally in the post-exponential phase of growth. Although secretion of exoproteins is not affected, an mutant is attenuated in a murine skin lesion model of pathogenicity.

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2004-02-01
2026-01-15

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References

  1. Akiyama Y., Ogura T., Ito K. 1994; Involvement of FtsH in protein assembly into and through the membrane. I. Mutations that reduce retention efficiency of a cytoplasmic reporter. J Biol Chem 269:5218–5224
    [Google Scholar]
  2. Akiyama Y., Kihara A., Ito K. 1996a; Subunit a of proton ATPase F0 sector is a substrate of the FtsH protease in Escherichia coli . FEBS Lett 399:26–28 [CrossRef]
    [Google Scholar]
  3. Akiyama Y., Kihara A., Tokuda H., Ito K. 1996b; FtsH (HflB) is an ATP-dependent protease selectively acting on SecY and some other membrane proteins. J Biol Chem 271:31196–31201 [CrossRef]
    [Google Scholar]
  4. Cassels R., Oliva B., Knowles D. 1995; Occurrence of the regulatory nucleotides ppGpp and pppGpp following induction of the stringent response in staphylococci. J Bacteriol 177:5161–5165
    [Google Scholar]
  5. Chan P. F., Foster S. J., Ingham E., Clements M. O. 1998; The Staphylococcus aureus alternative sigma factor σ B controls the environmental stress response but not starvation survival or pathogenicity in a mouse abscess model. J Bacteriol 180:6082–6089
    [Google Scholar]
  6. Clements M., Foster S. 1999; Stress resistance in Staphylococcus aureus . Trends Microbiol 7:458–462 [CrossRef]
    [Google Scholar]
  7. Clements M. O., Watson S. P., Foster S. J. 1999a; 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. Clements M. O., Watson S., Poole R. K., Foster S. J. 1999b; CtaA of Staphylococcus aureus is required for starvation survival, recovery, and cytochrome biosynthesis. J Bacteriol 181:501–507
    [Google Scholar]
  9. Deuerling E., Mogk A., Richter C., Purucker M., Schumann W. 1997; The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol Microbiol 23:921–933 [CrossRef]
    [Google Scholar]
  10. Fischer B., Rummel G., Aldridge P., Jenal U. 2002; The FtsH protease is involved in development, stress response and heat shock control in Caulobacter crescentus . Mol Microbiol 44:461–478 [CrossRef]
    [Google Scholar]
  11. Forsyth R. A., Haselbeck R. J., Ohlsen K. L. 20 other authors 2002; A genome-wide strategy for the identification of essential genes in Staphylococcus aureus . Mol Microbiol 43:1387–1400 [CrossRef]
    [Google Scholar]
  12. Ge Z., Taylor D. E. 1996; Sequencing, expression, and genetic characterization of the Helicobacter pylori ftsH gene encoding a protein homologous to members of a novel putative ATPase family. J Bacteriol 178:6151–6157
    [Google Scholar]
  13. Gentry D., Li T., Rosenberg M., McDevitt D. 2000; The rel gene is essential for in vitro growth of Staphylococcus aureus . J Bacteriol 182:4995–4997 [CrossRef]
    [Google Scholar]
  14. Guérout-Fleury A. M., Shazand K., Frandsen N., Stragier P. 1995; Antibiotic-resistance cassettes for Bacillus subtilis . Gene 167:335–336 [CrossRef]
    [Google Scholar]
  15. Herman C., Thevenet D., D'Ari R., Bouloc P. 1995; Degradation of σ 32, the heat shock regulator in Escherichia coli , is governed by HflB. Proc Natl Acad Sci U S A 92:3516–3520 [CrossRef]
    [Google Scholar]
  16. Horsburgh M. J., Aish J. L., White I. J., Shaw L., Lithgow J. K., Foster S. J. 2002a; σ B modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184:5457–5467 [CrossRef]
    [Google Scholar]
  17. Horsburgh M. J., Wharton S. J., Cox A. G., Ingham E., Peacock S., Foster S. J. 2002b; MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol Microbiol 44:1269–1286 [CrossRef]
    [Google Scholar]
  18. Kemp E. H., Sammons R. L., Moir A., Sun D., Setlow P. 1991; Analysis of transcriptional control of the gerD spore germination gene of Bacillus subtilis 168. J Bacteriol 173:4646–4652
    [Google Scholar]
  19. Kihara A., Akiyama Y., Ito K. 1995; FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc Natl Acad Sci U S A 92:4532–4536 [CrossRef]
    [Google Scholar]
  20. Kobayashi K., Ehrlich S. D., Albertini A. 96 other authors 2003; Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100:4678–4683 [CrossRef]
    [Google Scholar]
  21. Konarska-Kozlowska M., Iyer V. N. 1981; Physical and genetic organization of the IncN-group plasmid pCU1. Gene 14:195–204 [CrossRef]
    [Google Scholar]
  22. Kuroda M., Ohta T., Uchiyama I. 34 other authors 2001; Whole genome sequencing of methicillin-resistant Staphylococcus aureus . Lancet 357:1225–1240 [CrossRef]
    [Google Scholar]
  23. Langer T. 2000; AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem Sci 25:247–251 [CrossRef]
    [Google Scholar]
  24. Lowy F. D. 1998; Staphylococcus aureus infections. N Engl J Med 339:520–532 [CrossRef]
    [Google Scholar]
  25. Lysenko E., Ogura T., Cutting S. M. 1997; Characterization of the ftsH gene of Bacillus subtilis . Microbiology 143:971–978 [CrossRef]
    [Google Scholar]
  26. Nilsson D., Lauridsen A. A., Tomoyasu T., Ogura T. 1994; A Lactococcus lactis gene encodes a membrane protein with putative ATPase activity that is homologous to the essential Escherichia coli ftsH gene product. Microbiology 140:2601–2610 [CrossRef]
    [Google Scholar]
  27. Novick R. P. 1991; Genetic systems in staphylococci. Methods Enzymol 204:587–636
    [Google Scholar]
  28. Nygaard P. 1993; Purine and pyrimidine salvage pathways. In Bacillus subtilis and Other Gram-Positive Bacteria pp 359–378 Edited by Sonenshein A. L., Hoch J. A., Losick R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  29. Ogura T., Wilkinson A. J. 2001; AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6:575–597 [CrossRef]
    [Google Scholar]
  30. Ogura T., Tomoyasu T., Yuki T., Morimura S., Begg K. J., Donachie W. D., Mori H., Niki H., Hiraga S. 1991; Structure and function of the ftsH gene in Escherichia coli . Res Microbiol 142:279–282 [CrossRef]
    [Google Scholar]
  31. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Laboratory;
    [Google Scholar]
  32. Schenk S., Laddaga R. A. 1992; Improved method for electroporation of Staphylococcus aureus . FEMS Microbiol Lett 73:133–138
    [Google Scholar]
  33. Schumann W. 1999; FtsH – a single-chain charonin?. FEMS Microbiol Rev 23:1–11
    [Google Scholar]
  34. Shirai Y., Akiyama Y., Ito K. 1996; Suppression of ftsH mutant phenotypes by overproduction of molecular chaperones. J Bacteriol 178:1141–1145
    [Google Scholar]
  35. Taylor D. 1999; Bacterial tellurite resistance. Trends Microbiol 7:111–115 [CrossRef]
    [Google Scholar]
  36. Taylor C. M., Beresford M., Epton H. A., Sigee D. C., Shama G., Andrew P. W., Roberts I. S. 2002; Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J Bacteriol 184:621–628 [CrossRef]
    [Google Scholar]
  37. Tomoyasu T., Yuki T., Morimura S., Mori H., Yamanaka K., Niki H., Hiraga S., Ogura T. 1993; The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J Bacteriol 175:1344–1351
    [Google Scholar]
  38. Tomoyasu T., Gamer J., Bukau B. 9 other authors 1995; Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor σ 32. EMBO J 14:2551–2560
    [Google Scholar]
  39. Watson S. P., Antonio M., Foster S. J. 1998a; Isolation and characterization of Staphylococcus aureus starvation-induced, stationary-phase mutants defective in survival or recovery. Microbiology 144:3159–3169 [CrossRef]
    [Google Scholar]
  40. Watson S. P., Clements M. O., Foster S. J. 1998b; Characterization of the starvation-survival response of Staphylococcus aureus . J Bacteriol 180:1750–1758
    [Google Scholar]
  41. Zellmeier S., Zuber U., Schumann W., Wiegert T. 2003; The absence of FtsH metalloprotease activity causes overexpression of the σ W-controlled pbpE gene, resulting in filamentous growth of Bacillus subtilis . J Bacteriol 185:973–982 [CrossRef]
    [Google Scholar]
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