Magnesium transport in Salmonella typhimurium: biphasic magnesium and time dependence of the transcription of the mgtA and mgtCB loci

Microbiology (United Kingdom) - Tập 144 Số 3 - Trang 655-664 - 1998
Tao Tao1, Paul F. Grulich, Lisa M. Kucharski, Ronald L. Smith, Michael E. Maguire
1Department of Pharmacology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106-4965, USA

Tóm tắt

Salmonella typhimurium has three distinct Mg2+ transport systems, the constitutive high-capacity CorA transporter and two P-type ATPases, MgtA and MgtB, whose transcription is repressed by normal concentrations of Mg2+ in the growth medium. The latter Mg2+-transporting ATPase is part of a two-gene operon, mgtCB, with mgtC encoding a 23 kDa protein of unknown function. Transcriptional regulation using fusions of the promoter regions of mgtA and mgtCB to luxAB showed a biphasic time and Mg2+ concentration dependence. Between 1 and 6 h after transfer to nitrogen minimal medium containing defined concentrations of Mg2+, transcription increased about 200-fold for mgtCB and up to 400-fold for mgtA, each with a half-maximal dependence on Mg2+ of 0.5 mM. Continued incubation revealed a second phase of increased transcription, up to 2000-fold for mgtCB and up to 10000-fold for mgtA. This secondary increase occurred between 6 and 9 h after transfer to defined medium for mgtCB but between 12 and 24 h for mgtA and had a distinct half-maximal dependence for Mg2+ 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 Mg2+ was not dependent on a functional stationary-phase sigma factor encoded by rpoS, but it was dependent on the presence of a functional phoPQ two-component regulatory system. Whereas mgtCB was completely dependent on regulation via phoPQ, the secondary Sate Mg2+-dependent phase of mgtA transcription was still evident in strains carrying a mutation in either phoP or phoQ, albeit substantially diminished. Several divalent cations blocked the early phase of the increase in transcription elicited by the decrease in Mg2+ concentration, including cations that inhibit Mg2+ uptake (Co2+, Ni2+ and Mn2+) and those which do not (Ca2+ and Zn2+). 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 mgtA and mgtCB loci exist.

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Tài liệu tham khảo

Altendorf, 1994, Kdp-ATPase of Escherichia coli., Cell Physiol Biochem, 4, 160, 10.1159/000154719

Altura, 1992, Basic biochemistry and physiology of magnesium: a brief review., Magnesium Trace Elem, 10, 167

Clausen, 1991, Significance of cation transport in control of energy metabolism and thermogenesis., Physiol Rev, 71, 733, 10.1152/physrev.1991.71.3.733

Dosch, 1991, Genetic analysis of potassium transport loci in Escherichia coli: evidence for three constitutive systems mediating uptake of potassium., J Bacteriol, 173, 687, 10.1128/JB.173.2.687-696.1991

Epstein, 1993, Multiple mechanisms, roles and controls of K+ transport in Escherichia coli., Biochem Soc Trans, 21, 1006, 10.1042/bst0211006

Garcia-del Portillo, 1992, Characterization of the micro-environment of Salmonella typhimurium-containing vacuoles within MDCK epithelial cells., Mol Microbiol, 6, 3289, 10.1111/j.1365-2958.1992.tb02197.x

Garcia-Vescovi, 1996, Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence., Cell, 84, 165, 10.1016/S0092-8674(00)81003-X

Groisman, 1989, Salmonella typhimurium phoP virulence gene is a transcriptional regulator., Proc Natl Acad Sci USA, 86, 7077, 10.1073/pnas.86.18.7077

Gross, 1989, Pertussis toxin promoter sequences involved in modulation., J Bacteriol, 171, 4026, 10.1128/JB.171.7.4026-4030.1989

Grubbs, 1987, Magnesium as a regulatory cation: criteria and evaluation., Magnesium, 6, 113

Grubbs, 1985, Differential compartmentation of magnesium and calcium in murine S49 lymphoma cells., J Biol Chem, 259, 12184, 10.1016/S0021-9258(20)71337-2

Grubbs, 1989, Magnesium transport in eukaryotic and prokaryotic cells using magnesium-28 ion., Methods Enzymol, 173, 546, 10.1016/S0076-6879(89)73038-X

Gunn, 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, 10.1128/JB.178.23.6857-6864.1996

Guo, 1997, Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ., Science, 276, 250, 10.1126/science.276.5310.250

Guzzo, 1991, Transcription of the Escherichia coli fliC gene is regulated by metal ions., Appl Environ Microbiol, 57, 2255, 10.1128/AEM.57.8.2255-2259.1991

Hmiel, 1986, Magnesium transport in Salmonella typhimurium: characterization of magnesium influx and cloning of a transport gene., J Bacteriol, 168, 1444, 10.1128/JB.168.3.1444-1450.1986

Hmiel, 1989, Magnesium transport in Salmonella typhimurium: genetic characterization and cloning of three magnesium trans-port loci., J Bacteriol, 171, 4742, 10.1128/JB.171.9.4742-4751.1989

Johnston, 1996, Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response- regulator superfamily., Mol Microbiol, 22, 715, 10.1046/j.1365-2958.1996.d01-1719.x

Kertesz, 1993, Proteins induced by sulfate limitation in Escherichia coli, Pseudomonas putida, or Staphylococcus aureus., J Bacteriol, 175, 1187, 10.1128/JB.175.4.1187-1190.1993

Kiyota, 1989, Influence of magnesium concentration on production of exoprotein and β- lactamase by Staphylococcus aureus and Staphylococcus hemolyticus., J Infect Dis, 160, 1061, 10.1093/infdis/160.6.1061

Maguire, 1990, Magnesium: a regulated and regulatory cation., Metal Ions Biol, 26, 135

Maguire, 1992, Mg2+ transporting P-type ATPases of Salmonella typhimurium. Wrong way, wrong place enzymes., Ann NY Acad Sci, 671, 244, 10.1111/j.1749-6632.1992.tb43800.x

Miller, 1989, A two- component regulatory system (phoP-phoQ) controls Salmonella typhimurium virulence., Proc Natl Acad Sci USA, 86, 5054, 10.1073/pnas.86.13.5054

O’Halloran, 1993, Transition metals in control of gene expression., Science, 261, 715, 10.1126/science.8342038

Pedersen, 1987, Ion motive ATPases. I. Ubiquity, properties, and significance to cell function., Trends Biochem Sci, 12, 146, 10.1016/0968-0004(87)90071-5

Phinney, 1992, Regulation of expression by divalent cations of a light-inducible gene in Arthrobacter photo- gonimos., Arch Microbiol, 158, 85, 10.1007/BF00245210

Romani, 1993, Cell magnesium transport and homeostasis: role of intracellular compartments., Miner Electrolyte Metab, 19, 282

Scarlato, 1991, Differential response of the bvgvirulence regulon of Bordetella pertussis to MgSO4 modulation., J Bacteriol, 173, 7401, 10.1128/JB.173.22.7401-7404.1991

Smith, 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, 10.1016/S0021-9258(19)85210-9

Smith, 1993b, Membrane topology of a P-type ATPase: the MgtB Mg2+ transport protein of Salmonella typhimurium., J Biol Chem, 268, 22469, 10.1016/S0021-9258(18)41553-0

Snavely, 1989, Magnesium transport in Salmonella typhimurium: 28Mg2+ transport by the CorA, MgtA, and MgtB systems., J Bacteriol, 171, 4761, 10.1128/JB.171.9.4761-4766.1989

Snavely, 1991a, The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P- type ATPase., J Biol Chem, 266, 815, 10.1016/S0021-9258(17)35246-8

Snavely, 1991b, Magnesium transport in Salmonella typhimurium: regulation of mgtA and mgtB expression., J Biol Chem, 266, 824, 10.1016/S0021-9258(17)35247-X

Soncini, 1996, Two-component regu-latory systems can interact to process multiple environmental signals., J Bacteriol, 178, 6796, 10.1128/JB.178.23.6796-6801.1996

Soncini, 1996, Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes., J Bacteriol, 178, 5092, 10.1128/JB.178.17.5092-5099.1996

Tao, 1995, Magnesium transport in Salmonella typhimurium: the mgtA locus encodes a P-type ATPase regulated similarly to mgtB., J Bacteriol, 177, 2663, 10.1128/JB.177.10.2654-2662.1995

Vescovi, 1997, Characterization of the bacterial sensor protein PhoQ. Evidence for distinct binding sites for Mg2+ and Ca2+., J Biol Chem, 272, 1440, 10.1074/jbc.272.3.1440

Wilmes-Riesenberg, 1997, Analtered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2., Infect Immun, 65, 203, 10.1128/IAI.65.1.203-210.1997