Abstract
Escherichia coli genes regulated by environmental inorganic phosphate (Pi) levels form the phosphate (Pho) regulon. This regulation requires seven proteins, whose synthesis is under autogenous control, including response regulator PhoB, its partner, histidine sensor kinase PhoR, all four components of the Pi-specific transport (Pst) system (PstA, PstB, PstC, and PstS), and a protein of unknown function called PhoU. Here we examined the effects of uncoupling PhoB synthesis and PhoR synthesis from their normal controls by placing each under the tight control of the arabinose-regulated P(araB) promoter or the rhamnose-regulated P(rhaB) promoter. To do this, we made allele replacement plasmids that may be generally useful for construction of P(araB) or P(rhaB) fusions and for recombination of them onto the E. coli chromosome at the araCBAD or rhaRSBAD locus, respectively. Using strains carrying such single-copy fusions, we showed that a P(rhaB) fusion is more tightly regulated than a P(araB) fusion in that a P(rhaB)-phoR+ fusion but not a P(araB)-phoR+ fusion shows a null phenotype in the absence of its specific inducer. Yet in the absence of induction, both P(araB)-phoB+ and P(rhaB)-phoB+ fusions exhibit a null phenotype. These data indicate that less PhoR than PhoB is required for transcriptional activation of the Pho regulon, which is consistent with their respective modes of action. We also used these fusions to study PhoU. Previously, we had constructed strains with precise delta phoU mutations. However, we unexpectedly found that such delta phoU mutants have a severe growth defect (P. M. Steed and B. L. Wanner, J. Bacteriol. 175:6797-6809, 1993). They also readily give rise to compensatory mutants with lesions in phoB, phoR, or a pst gene, making their study particularly difficult. Here we found that, by using P(araB)-phoB+, P(rhaB)-phoB+, or P(rhaB)-phoR+ fusions, we were able to overcome the extremely deleterious growth defect of a Pst+ delta phoU mutant. The growth defect is apparently a consequence of high-level Pst synthesis resulting from autogenous control of PhoB and PhoR synthesis in the absence of PhoU.
MeSH Terms
Arabinose/genetics,metabolism
Artificial Gene Fusion
Bacterial Proteins/biosynthesis,genetics,physiology
Escherichia coli/genetics,growth & development,metabolism
Escherichia coli Proteins
Gene Expression Regulation, Bacterial
Genetic Vectors
Lac Operon
Membrane Transport Proteins
Mutation
Phosphates/metabolism
Promoter Regions, Genetic
Regulon
Rhamnose/genetics,metabolism
Transcription Factors/biosynthesis,genetics
Chemicals
Bacterial Proteins
Escherichia coli Proteins
Membrane Transport Proteins
Phosphates
Transcription Factors
phoU protein, E coli
PhoB protein, Bacteria
PhoR protein, Bacteria
Arabinose
Rhamnose
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Haldimann A
Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907, USA.
Daniels L L
Wanner B L
References (25)
25 references, click to expand
-
Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant.
Gene. 1995 May 26;158(1):9-14
PMID: 7789817
-
A regulatory cascade in the induction of rhaBAD.
J Mol Biol. 1993 Nov 5;234(1):87-98
PMID: 8230210
-
Cross-talk between the histidine protein kinase VanS and the response regulator PhoB. Characterization and identification of a VanS domain that inhibits activation of PhoB.
J Biol Chem. 1995 Sep 29;270(39):23143-9
PMID: 7559459
-
Kinetic comparison of the specificity of the vancomycin resistance VanSfor two response regulators, VanR and PhoB.
Biochemistry. 1996 Apr 16;35(15):4732-40
PMID: 8664263
-
Conditionally replicative and conjugative plasmids carrying lacZ alpha for cloning, mutagenesis, and allele replacement in bacteria.
Plasmid. 1996 Jan;35(1):1-13
PMID: 8693022
-
Altered recognition mutants of the response regulator PhoB: a new genetic strategy for studying protein-protein interactions.
Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14361-6
PMID: 8962056
-
Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations.
Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8168-72
PMID: 9223333
-
Transcriptional regulation of the Enterococcus faecium BM4147 vancomycin resistance gene cluster by the VanS-VanR two-component regulatory system in Escherichia coli K-12.
J Bacteriol. 1997 Sep;179(18):5903-13
PMID: 9294451
-
Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria.
J Bacteriol. 2001 Nov;183(21):6384-93
PMID: 11591683
-
Adenosine 3':5'-cyclic monophosphate as mediator of catabolite repression in Escherichia coli.
Proc Natl Acad Sci U S A. 1975 Jun;72(6):2300-4
PMID: 166384
-
Overlapping and separate controls on the phosphate regulon in Escherichia coli K12.
J Mol Biol. 1983 May 25;166(3):283-308
PMID: 6304324
-
Analysis of regulation of phoB expression using a phoB-cat fusion.
J Bacteriol. 1983 Nov;156(2):710-7
PMID: 6313614
-
Kanamycin-resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9.
Gene. 1986;41(2-3):337-42
PMID: 3011607
-
The phoBR operon in Escherichia coli K-12.
J Bacteriol. 1987 Dec;169(12):5569-74
PMID: 2824439
-
Accumulation of trehalose by Escherichia coli K-12 at high osmotic pressure depends on the presence of amber suppressors.
J Bacteriol. 1988 Aug;170(8):3601-10
PMID: 3042755
-
Mapping and molecular cloning of the phn (psiD) locus for phosphonate utilization in Escherichia coli.
J Bacteriol. 1990 Mar;172(3):1186-96
PMID: 2155195
-
The three operators of the lac operon cooperate in repression.
EMBO J. 1990 Apr;9(4):973-9
PMID: 2182324
-
Cloning, mapping and gene product identification of rhaT from Escherichia coli K12.
FEMS Microbiol Lett. 1990 Oct;60(1-2):103-7
PMID: 2283027
-
Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli.
J Bacteriol. 1992 Apr;174(7):2124-30
PMID: 1551836
-
The E. coli ffh gene is necessary for viability and efficient protein export.
Nature. 1992 Oct 22;359(6397):744-6
PMID: 1331806
-
Mutational analysis of the Escherichia coli phosphate-specific transport system, a member of the traffic ATPase (or ABC) family of membrane transporters. A role for proline residues in transmembrane helices.
J Biol Chem. 1992 Dec 5;267(34):24661-8
PMID: 1447208
-
Role of PhoU in phosphate transport and alkaline phosphatase regulation.
J Bacteriol. 1992 Dec;174(24):8057-64
PMID: 1459954
-
Mutational analysis of an Escherichia coli fourteen-gene operon for phosphonate degradation, using TnphoA' elements.
J Bacteriol. 1993 Jun;175(11):3430-42
PMID: 8388873
-
Use of the rep technique for allele replacement to construct mutants with deletions of the pstSCAB-phoU operon: evidence of a new role for the PhoU protein in the phosphate regulon.
J Bacteriol. 1993 Nov;175(21):6797-809
PMID: 8226621
-
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
J Bacteriol. 1995 Jul;177(14):4121-30
PMID: 7608087