Osmotic regulation of transcription: induction of the proU betaine transport gene is dependent on accumulation of intracellular potassium

Sutherland, Lesley; Cairney, John; Elmore, M; Booth, Ian R.; Higgins, Christopher F.

doi:10.1128/jb.168.2.805-814.1986

Cited by 219 publications

(181 citation statements)

References 45 publications

(46 reference statements)

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“…Thus cells grown in 200 mM-NaCl showed negligible increases in internal proline concentration but significant increases in K+ concentration over the same range (Whatmore, 1989). However, if upshock is more substantial, accumulation of K+ will lead to induction and/or activation of proline biosynthetic enzymes, since accumulation of excessive K+ may be potentially deleterious to cellular metabolism (Sutherland et al, 1986;Booth et al, 1988). K+ has now been shown to exert its effects in upshocked enteric bacteria via the induction of glycine betaine uptake (proU-mediated) due to alteration of DNA structure.…”

Section: Discussionmentioning

confidence: 99%

The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis

Whatmore

Chudek²,

Reed

1990

Journal of General Microbiology

261

327

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The effects of hypersaline treatment (osmotic upshock) on solute accumulation have been studied in the Grampositive bacterium BaciZZus subtiZis. Natural abundance 3C NMR spectroscopy studies revealed only proline as a major organic osmoticum in cells grown in defined medium (no exogenous organic solutes) and this finding was confirmed by amino acid analysis. Intracellular concentrations of both K+ and proline rose markedly after osmotic upshock. K+ influx from the medium was rapid (< 1 h) but proline synthesis was a slower process (5-9 h). Proline synthesis appeared to be dependent on the prior accumulation of K+ and it is possible that K+ serves in some manner as the signal for increased proline synthesis. In cells upshocked in medium enriched in glycine betaine the endogenous synthesis of proline was repressed and glycine betaine served as the sole organic osmoticum. K+ was also accumulated under these conditions.

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Section: Discussionmentioning

confidence: 99%

The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis

Whatmore

Chudek²,

Reed

1990

Journal of General Microbiology

261

327

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“…Control by turgor is supported by the finding that a sudden increase in medium osmolarity, which reduces turgor, transiently turns on kdp-FABC expression. This model has been challenged by the finding that under some conditions expression of kdpFABC is only significantly induced when the osmolarity of the medium is increased by salt and not in case of sugar (9,14,15). Based on kdpD mutants, which give rise to K ϩ -independent kdpFABC expression but regain the ability to respond to changes in medium osmolarity independently of the solute, it is suggested that KdpD senses two stimuli: increase in osmolarity and K ϩ limitation (16).…”

Section: ) (3)mentioning

confidence: 99%

The Hydrophilic N-terminal Domain Complements the Membrane-anchored C-terminal Domain of the Sensor Kinase KdpD ofEscherichia coli

Heermann

Altendorf

Jung

2000

Journal of Biological Chemistry

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“…Because of difficulties in obtaining kdp mutations in this organism, it has been suggested that there may be an important difference between the properties of the Kdp system in E. coli and in S. typhimurium (17). In this report, we describe the isolation of a kdp-lacZ fusion in S. typhimurium.…”

mentioning

confidence: 96%

Characterization of transcriptional regulation of the kdp operon of Salmonella typhimurium

et al. 1997

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The transcriptional control of the kdpFABC (K ؉ transport) operon of Salmonella typhimurium was characterized with a lacZ fusion. The kdpFABC operon of this organism was induced by K ؉ limitation and high osmolality, and osmotic induction was antagonized by a high concentration of K ؉ . In the trkA (sapG) kdp ؉ mutant background, high concentrations of K ؉ inhibited growth, along with repressing the kdp operon. This result, which has not been reported for Escherichia coli, is inconsistent with the model in which the signal for the induction of the kdp operon is turgor loss.In enteric bacteria, K ϩ is taken up by two major permeases, Trk and Kdp, and by a minor permease, Kup (13,18). In Escherichia coli, the activity of these three systems has been shown to be stimulated by osmotic stress (2). Stimulation of Kdp is effected largely by transcriptional induction of the kdpFABC operon. The kdpFABC operon is also induced by K ϩ limitation. Transcriptional control of the kdpFABC operon is mediated by the KdpD and KdpE proteins (2), which belong to the family of two-component regulatory proteins. It has been proposed that the regulatory signal for the expression of the kdp operon is turgor (4), but whether the osmotic-stress-and the K ϩ -dependent regulations are mediated by a single mechanism or by two distinct mechanisms is controversial (1, 2, 6, 7).The regulation of the kdp operon in Salmonella typhimurium has not been studied. Because of difficulties in obtaining kdp mutations in this organism, it has been suggested that there may be an important difference between the properties of the Kdp system in E. coli and in S. typhimurium (17). In this report, we describe the isolation of a kdp-lacZ fusion in S. typhimurium.Strain construction. The medium used for the isolation of the kdp-lacZ mutations was K0 medium (5), which has a K ϩ concentration of 0.1 mM (introduced as a trace contaminant in other chemicals). Approximately 5,000 derivatives of the wildtype S. typhimurium strain LT2 carrying random MudI1734 (Km lac) insertions (10) were replica plated to K0 plates containing 10 mM glucose, kanamycin, and 40 mg of X-Gal (5-bromo-4-chloro-3-indolyl-␤-D-galactopyranoside) per liter (12) and to plates containing the same ingredients plus 10 mM KCl. We identified one derivative, strain TL2626, which formed a very small, dark blue colony on the former medium and a normal-sized, white colony on the latter; the mutation in this strain was designated kdp-101::MudI1734.P22 transductions (3) demonstrated that the kdp-101:: MudI1734 insertion was 96% linked and was located upstream of a kdp::Tn10 insertion (obtained from E. Groisman) (data not shown). In Southern blot analyses, a fragment containing the kdpFABC operon of E. coli exhibited different patterns of hybridization to EcoRI, EcoRV, PvuII, and HincII fragments of the DNA from strain TL2626 than to those from strain LT2 (data not shown). The kdp-101::MudI1734 insertion was complemented by a plasmid which expressed the kdpB ϩ C ϩ genes of E. coli (obtained from W. Epstein)...

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Osmotic regulation of transcription: induction of the proU betaine transport gene is dependent on accumulation of intracellular potassium

Cited by 219 publications

References 45 publications

The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis

The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis

The Hydrophilic N-terminal Domain Complements the Membrane-anchored C-terminal Domain of the Sensor Kinase KdpD ofEscherichia coli

Characterization of transcriptional regulation of the kdp operon of Salmonella typhimurium

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