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Volume 144, Issue 3

Magnesium transport in : biphasic magnesium and time dependence of the transcription of the and loci Free

Abstract

has three distinct Mg transport systems, the constitutive high-capacity CorA transporter and two P-type ATPases, MgtA and MgtB, whose transcription is repressed by normal concentrations of Mg in the growth medium. The latter Mg-transporting ATPase is part of a two-gene operon, , with encoding a 23 kDa protein of unknown function. Transcriptional regulation using fusions of the promoter regions of and to showed a biphasic time and Mg concentration dependence. Between 1 and 6 h after transfer to nitrogen minimal medium containing defined concentrations of Mg, transcription increased about 200-fold for and up to 400-fold for , each with a half-maximal dependence on Mg of 0.5 mM. Continued incubation revealed a second phase of increased transcription, up to 2000-fold for and up to 10000-fold for . This secondary increase occurred between 6 and 9 h after transfer to defined medium for but between 12 and 24 h for and had a distinct half-maximal dependence for Mg of 0.01 mM. A concomitant increase of at least 1000-fold in uptake of cation was seen between 8 and 24 h incubation with either system, showing that the transcriptional increase was followed by functional incorporation of large amounts of the newly synthesized transporter into the membrane. Regulation of transcription by Mg was not dependent on a functional stationary-phase sigma factor encoded by , but it was dependent on the presence of a functional two-component regulatory system. Whereas was completely dependent on regulation via , the secondary Sate Mg-dependent phase of transcription was still evident in strains carrying a mutation in either or , albeit substantially diminished. Several divalent cations blocked the early phase of the increase in transcription elicited by the decrease in Mg concentration, including cations that inhibit Mg uptake (Co, Ni and Mn) and those which do not (Ca and Zn). In contrast, the second later phase of the transcriptional increase was not well blocked by any cation except those which inhibit uptake. Overall, the data suggest that at least two distinct mechanisms for transcriptional regulation of the and loci exist.

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Keyword(s): magnesium regulation , magnesium transport , phoPQ two-component system and Salmonella typhimurium
© Society for General Mcrobiology 1998
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1998-03-01
2024-04-16
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References

  1. Altendorf K., Epstein W. 1994; Kdp-ATPase of Escherichia coli.. Cell Physiol Biochem 4:160–168
     [Google Scholar]
  2. Altura B.M. 1992; Basic biochemistry and physiology of magnesium: a brief review.. Magnesium Trace Elem 10:167–171
     [Google Scholar]
  3. Clausen T., Van Hardeveld C., Everts M.E. 1991; Significance of cation transport in control of energy metabolism and thermogenesis.. Physiol Rev 71:733–774
     [Google Scholar]
  4. Dosch D.C., Helmer G.L., Sutton S.H., Salvacion F.F., Epstein W. 1991; Genetic analysis of potassium transport loci in Escherichia coli: evidence for three constitutive systems mediating uptake of potassium.. J Bacteriol 173:687–696
     [Google Scholar]
  5. Epstein W., Buurman E., McLaggan D., Naprstek J. 1993; Multiple mechanisms, roles and controls of K+ transport in Escherichia coli.. Biochem Soc Trans 21:1006–1010
     [Google Scholar]
  6. Garcia-del Portillo F., Foster J.W., Maguire M.E., Finlay B.B. 1992; Characterization of the micro-environment of Salmonella typhimurium-containing vacuoles within MDCK epithelial cells.. Mol Microbiol 6:3289–3297
     [Google Scholar]
  7. Garcia-Vescovi E., Soncini F.C., Groisman E.A. 1996; Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence.. Cell 84:165–174
     [Google Scholar]
  8. Groisman E.A., Chiao E., Lipps C.J., Heffron F. 1989; Salmonella typhimurium phoP virulence gene is a transcriptional regulator.. Proc Natl Acad Sci USA 86:7077–7081
     [Google Scholar]
  9. Gross R., Rappuoli R. 1989; Pertussis toxin promoter sequences involved in modulation.. J Bacteriol 171:4026–4030
     [Google Scholar]
  10. Grubbs R.D., Maguire M.E. 1987; Magnesium as a regulatory cation: criteria and evaluation.. Magnesium 6:113–127
     [Google Scholar]
  11. Grubbs R.D., Collins S.D. 1985; Differential compartmentation of magnesium and calcium in murine S49 lymphoma cells.. J Biol Chem 259:12184–12192
     [Google Scholar]
  12. Grubbs R.D., Snavely M.D., Hmiel S.P. 1989; Magnesium transport in eukaryotic and prokaryotic cells using magnesium-28 ion.. Methods Enzymol 173:546–563
     [Google Scholar]
  13. Gunn J.S., Miller S.I. 1996; PhoP-PhoQ activates tran-scription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance.. J Bacteriol 178:6857–6864
     [Google Scholar]
  14. Guo L., Lim K.B., Gunn J.S., Bainbridge B., Darveau R.P., Hackett M., Mileer S.I. 1997; Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ.. Science 276:250–253
     [Google Scholar]
  15. Guzzo A., Diorio C., Dubow M.S. 1991; Transcription of the Escherichia coli fliC gene is regulated by metal ions.. Appl Environ Microbiol 57:2255–2259
     [Google Scholar]
  16. Hmiel S.P., Snavely M.D., Miller C.G., Maguire M.E. 1986; Magnesium transport in Salmonella typhimurium: characterization of magnesium influx and cloning of a transport gene.. J Bacteriol 168:1444–1450
     [Google Scholar]
  17. Hmiel S.P., Snavely M.D., Florer J.B., Maguire M.E., Miller C.G. 1989; Magnesium transport in Salmonella typhimurium: genetic characterization and cloning of three magnesium trans-port loci.. J Bacteriol 171:4742–4751
     [Google Scholar]
  18. Johnston C., Pegues D.A., Hueck C.J., Lee A., Miller S.I. 1996; Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response- regulator superfamily.. Mol Microbiol 22:715–727
     [Google Scholar]
  19. Kertesz M.A., Leisinger T., Cook A.M. 1993; Proteins induced by sulfate limitation in Escherichia coli, Pseudomonas putida, or Staphylococcus aureus.. J Bacteriol 175:1187–1190
     [Google Scholar]
  20. Kiyota H., Kendrick M.I., Kass E.H. 1989; Influence of magnesium concentration on production of exoprotein and β- lactamase by Staphylococcus aureus and Staphylococcus hemolyticus.. J Infect Dis 160:1061–1063
     [Google Scholar]
  21. Maguire M.E. 1990; Magnesium: a regulated and regulatory cation.. Metal Ions Biol 26:135–153
     [Google Scholar]
  22. Maguire M.E., Snavely M.D., Leizman J.B., Gura S., Bagga D., Tao T., Smith D.L. 1992; Mg2+ transporting P-type ATPases of Salmonella typhimurium. Wrong way, wrong place enzymes.. Ann NY Acad Sci 671:244–256
     [Google Scholar]
  23. Miller S.I., Kukral A.M., Mekalanos J.J. 1989; A two- component regulatory system (phoP-phoQ) controls Salmonella typhimurium virulence.. Proc Natl Acad Sci USA 86:5054–5058
     [Google Scholar]
  24. O’Halloran T.V. 1993; Transition metals in control of gene expression.. Science 261:715–725
     [Google Scholar]
  25. Pedersen P.L., Carafoli E. 1987; Ion motive ATPases. I. Ubiquity, properties, and significance to cell function.. Trends Biochem Sci 12:146–150
     [Google Scholar]
  26. Phinney D.G., Hoober J.K. 1992; Regulation of expression by divalent cations of a light-inducible gene in Arthrobacter photo- gonimos.. Arch Microbiol 158:85–92
     [Google Scholar]
  27. Romani A., Marfella C., Scarpa A. 1993; Cell magnesium transport and homeostasis: role of intracellular compartments.. Miner Electrolyte Metab 19:282–289
     [Google Scholar]
  28. Scarlato V., Rappuoii R. 1991; Differential response of the bvgvirulence regulon of Bordetella pertussis to MgSO4 modulation.. J Bacteriol 173:7401–7404
     [Google Scholar]
  29. Smith R.L., Banks J.L., Snavely M.D., Maguire M.E. 1993a; Sequence and topology of the CorA magnesium transport systems of Salmonella typhimurium and Escherichia coli. Identification of a new class of transport protein.. J Biol Chem 268:14071–14080
     [Google Scholar]
  30. Smith D.L., Tao T., Maguire M.E. 1993b; Membrane topology of a P-type ATPase: the MgtB Mg2+ transport protein of Salmonella typhimurium.. J Biol Chem 268:22469–22479
     [Google Scholar]
  31. Snavely M.D., Florer J.B., Miller C.G., Maguire M.E. 1989; Magnesium transport in Salmonella typhimurium: 28Mg2+ transport by the CorA, MgtA, and MgtB systems.. J Bacteriol 171:4761–4766
     [Google Scholar]
  32. Snavely M.D., Miller C.G., Maguire M.E. 1991a; The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P- type ATPase.. J Biol Chem 266:815–823
     [Google Scholar]
  33. Snavely M.D., Gravina S.A., Cheung T.T., Miller C.G., Maguire M.E. 1991b; Magnesium transport in Salmonella typhimurium: regulation of mgtA and mgtB expression.. J Biol Chem 266:824–829
     [Google Scholar]
  34. Soncini F.C., Groisman E.A. 1996; Two-component regu-latory systems can interact to process multiple environmental signals.. J Bacteriol 178:6796–6801
     [Google Scholar]
  35. Soncini F.C., Garcia-Vescovi E., Solomon F., Groisman E.A. 1996; Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes.. J Bacteriol 178:5092–5099
     [Google Scholar]
  36. Tao T., Snavely M.D., Gura S., Maguire M.E. 1995; Magnesium transport in Salmonella typhimurium: the mgtA locus encodes a P-type ATPase regulated similarly to mgtB.. J Bacteriol 177:2663–2672
     [Google Scholar]
  37. Vescovi E.G., Ayala Y., Di Cera E., Groisman E.A. 1997; Characterization of the bacterial sensor protein PhoQ. Evidence for distinct binding sites for Mg2+ and Ca2+.. J Biol Chem 272:1440–1443
     [Google Scholar]
  38. Wilmes-Riesenberg M.R., Foster J.W., Curtiss R. III 1997; Analtered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2.. Infect Immun 65:203–210
     [Google Scholar]
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Magnesium transport in Salmonella typhimurium: biphasic magnesium and time dependence of the transcription of the mgtA and mgtCB loci
Microbiology 144, 655 (1998); https://doi.org/10.1099/00221287-144-3-655
/content/journal/micro/10.1099/00221287-144-3-655
/content/journal/micro/10.1099/00221287-144-3-655
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