Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 May;177(10):2654–2662. doi: 10.1128/jb.177.10.2654-2662.1995

Magnesium transport in Salmonella typhimurium: mgtA encodes a P-type ATPase and is regulated by Mg2+ in a manner similar to that of the mgtB P-type ATPase.

T Tao 1, M D Snavely 1, S G Farr 1, M E Maguire 1
PMCID: PMC176934  PMID: 7751273

Abstract

Salmonella typhimurium has three distinct Mg2+ transport systems: CorA, MgtA, and MgtB, each encoded by its respective gene. corA and mgtB have been previously sequenced and characterized. This report details the sequence and properties of mgtA. Like mgtB, mgtA encodes a P-type ATPase. The mgtA gene encodes a slightly smaller protein than does mgtB, with a predicted molecular mass of about 95 kDa, running at 91 kDa on protein gels, which compares with values of 101 and 102 kDa, respectively, for the MgtB protein. The deduced amino acid sequence of MgtA is only 50% identical to that of MgtB, with a further 25% conservative amino acid substitutions, surprisingly low for such otherwise functionally similar proteins from the same organism. Codon usage for each gene is normal for S. typhimurium, however, indicating that neither gene is the result of a recent acquisition from another organism. A single open reading frame at mgtA encodes MgtA, in contrast to mgtB, which is shown to be an operon encoding (5' to 3') the 22.5-kDa MgtC and the MgtB proteins. Genetic constructs were used to show that deletion of MgtC does not alter the expression or transport properties of MgtB, making the role of the companion MgtC protein unclear. (The S. typhimurium homolog of treR, which encodes a putative repressor for trehalose uptake, is encoded by a gene adjacent to mgtA, and its sequence is also reported. Finally, exteremely strong Mg(2+) regulation of the mgtA and mgtB promoters but not of the corA or treR promoters was demonstrated by cloning the appropriate DNA sequences with luxAB and measuring enhancement of light production as a function of extracellular Mg(2+) concentration. Lowering the extracellular Mg(2+) concentration from 10 mM to 1 or 10 microM elicited a transcriptional response of several thousandfold from both the mgtA and mgtB promoters.

Full Text

The Full Text of this article is available as a PDF (522.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Altura B. M. Basic biochemistry and physiology of magnesium: a brief review. Magnes Trace Elem. 1991;10(2-4):167–171. [PubMed] [Google Scholar]
  3. Bakker E. P., Booth I. R., Dinnbier U., Epstein W., Gajewska A. Evidence for multiple K+ export systems in Escherichia coli. J Bacteriol. 1987 Aug;169(8):3743–3749. doi: 10.1128/jb.169.8.3743-3749.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clausen T., Van Hardeveld C., Everts M. E. Significance of cation transport in control of energy metabolism and thermogenesis. Physiol Rev. 1991 Jul;71(3):733–774. doi: 10.1152/physrev.1991.71.3.733. [DOI] [PubMed] [Google Scholar]
  5. Demple B. Regulation of bacterial oxidative stress genes. Annu Rev Genet. 1991;25:315–337. doi: 10.1146/annurev.ge.25.120191.001531. [DOI] [PubMed] [Google Scholar]
  6. Dosch D. C., Helmer G. L., Sutton S. H., Salvacion F. F., Epstein W. Genetic analysis of potassium transport loci in Escherichia coli: evidence for three constitutive systems mediating uptake potassium. J Bacteriol. 1991 Jan;173(2):687–696. doi: 10.1128/jb.173.2.687-696.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Epstein W., Buurman E., McLaggan D., Naprstek J. Multiple mechanisms, roles and controls of K+ transport in Escherichia coli. Biochem Soc Trans. 1993 Nov;21(4):1006–1010. doi: 10.1042/bst0211006. [DOI] [PubMed] [Google Scholar]
  8. Flatman P. W. Mechanisms of magnesium transport. Annu Rev Physiol. 1991;53:259–271. doi: 10.1146/annurev.ph.53.030191.001355. [DOI] [PubMed] [Google Scholar]
  9. Garcia-del Portillo F., Foster J. W., Maguire M. E., Finlay B. B. Characterization of the micro-environment of Salmonella typhimurium-containing vacuoles within MDCK epithelial cells. Mol Microbiol. 1992 Nov;6(22):3289–3297. doi: 10.1111/j.1365-2958.1992.tb02197.x. [DOI] [PubMed] [Google Scholar]
  10. Geering K. Subunit assembly and functional maturation of Na,K-ATPase. J Membr Biol. 1990 May;115(2):109–121. doi: 10.1007/BF01869450. [DOI] [PubMed] [Google Scholar]
  11. Geering K. Subunit assembly and posttranslational processing of Na(+)-pumps. Acta Physiol Scand Suppl. 1992;607:177–181. [PubMed] [Google Scholar]
  12. Grubbs R. D., Collins S. D., Maguire M. E. Differential compartmentation of magnesium and calcium in murine S49 lymphoma cells. J Biol Chem. 1984 Oct 10;259(19):12184–12192. [PubMed] [Google Scholar]
  13. Grubbs R. D., Maguire M. E. Magnesium as a regulatory cation: criteria and evaluation. Magnesium. 1987;6(3):113–127. [PubMed] [Google Scholar]
  14. Grubbs R. D., Snavely M. D., Hmiel S. P., Maguire M. E. Magnesium transport in eukaryotic and prokaryotic cells using magnesium-28 ion. Methods Enzymol. 1989;173:546–563. doi: 10.1016/s0076-6879(89)73038-x. [DOI] [PubMed] [Google Scholar]
  15. Hmiel S. P., Snavely M. D., Florer J. B., Maguire M. E., Miller C. G. Magnesium transport in Salmonella typhimurium: genetic characterization and cloning of three magnesium transport loci. J Bacteriol. 1989 Sep;171(9):4742–4751. doi: 10.1128/jb.171.9.4742-4751.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maguire M. E. Magnesium and cell proliferation. Ann N Y Acad Sci. 1988;551:201–217. doi: 10.1111/j.1749-6632.1988.tb22338.x. [DOI] [PubMed] [Google Scholar]
  17. Matsuda H. Magnesium gating of the inwardly rectifying K+ channel. Annu Rev Physiol. 1991;53:289–298. doi: 10.1146/annurev.ph.53.030191.001445. [DOI] [PubMed] [Google Scholar]
  18. Mircheff A. K., Bowen J. W., Yiu S. C., McDonough A. A. Synthesis and translocation of Na(+)-K(+)-ATPase alpha- and beta-subunits to plasma membrane in MDCK cells. Am J Physiol. 1992 Feb;262(2 Pt 1):C470–C483. doi: 10.1152/ajpcell.1992.262.2.C470. [DOI] [PubMed] [Google Scholar]
  19. Park S. F., Stirling D. A., Hulton C. S., Booth I. R., Higgins C. F., Stewart G. S. A novel, non-invasive promoter probe vector: cloning of the osmoregulated proU promoter of Escherichia coli K12. Mol Microbiol. 1989 Aug;3(8):1011–1023. doi: 10.1111/j.1365-2958.1989.tb00252.x. [DOI] [PubMed] [Google Scholar]
  20. Reinhart R. A. Magnesium metabolism. A review with special reference to the relationship between intracellular content and serum levels. Arch Intern Med. 1988 Nov;148(11):2415–2420. doi: 10.1001/archinte.148.11.2415. [DOI] [PubMed] [Google Scholar]
  21. Romani A., Marfella C., Scarpa A. Cell magnesium transport and homeostasis: role of intracellular compartments. Miner Electrolyte Metab. 1993;19(4-5):282–289. [PubMed] [Google Scholar]
  22. Ryan M. P. Interrelationships of magnesium and potassium homeostasis. Miner Electrolyte Metab. 1993;19(4-5):290–295. [PubMed] [Google Scholar]
  23. Serrano R., Portillo F., Monk B. C., Palmgren M. G. The regulatory domain of fungal and plant plasma membrane H(+)-ATPase. Acta Physiol Scand Suppl. 1992;607:131–136. [PubMed] [Google Scholar]
  24. Smith D. L., Maguire M. E. Molecular aspects of Mg2+ transport systems. Miner Electrolyte Metab. 1993;19(4-5):266–276. [PubMed] [Google Scholar]
  25. Smith D. L., Tao T., Maguire M. E. Membrane topology of a P-type ATPase. The MgtB magnesium transport protein of Salmonella typhimurium. J Biol Chem. 1993 Oct 25;268(30):22469–22479. [PubMed] [Google Scholar]
  26. Smith R. L., Banks J. L., Snavely M. D., Maguire M. E. 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. 1993 Jul 5;268(19):14071–14080. [PubMed] [Google Scholar]
  27. Snavely M. D., Florer J. B., Miller C. G., Maguire M. E. Magnesium transport in Salmonella typhimurium: 28Mg2+ transport by the CorA, MgtA, and MgtB systems. J Bacteriol. 1989 Sep;171(9):4761–4766. doi: 10.1128/jb.171.9.4761-4766.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Snavely M. D., Florer J. B., Miller C. G., Maguire M. E. Magnesium transport in Salmonella typhimurium: expression of cloned genes for three distinct Mg2+ transport systems. J Bacteriol. 1989 Sep;171(9):4752–4760. doi: 10.1128/jb.171.9.4752-4760.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Snavely M. D., Gravina S. A., Cheung T. T., Miller C. G., Maguire M. E. Magnesium transport in Salmonella typhimurium. Regulation of mgtA and mgtB expression. J Biol Chem. 1991 Jan 15;266(2):824–829. [PubMed] [Google Scholar]
  30. Snavely M. D., Miller C. G., Maguire M. E. The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem. 1991 Jan 15;266(2):815–823. [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES