Induction of the Pho regulon suppresses the growth defect of an Escherichia coli sgrS mutant, connecting phosphate metabolism to the glucose-phosphate stress response

Gregory R. Richards, Carin K. Vanderpool

Research output: Contribution to journalArticle

Abstract

Some bacteria experience stress when glucose-6-phosphate or analogues like α-methyl glucoside-6-phosphate (αMG6P) accumulate in the cell. In Escherichia coli, the small SgrS RNA is vital to recovery from glucose-phosphate stress; the growth of sgrS mutants is strongly inhibited by αMG. SgrS helps to restore growth in part through inhibiting translation of the ptsG mRNA, which encodes the major glucose transporter EIICBGlc. While the regulatory mechanism of SgrS has been characterized, little is known about how glucose-phosphate stress connects to other aspects of cell physiology. In the present study, we discovered that mutation of pitA, which encodes the low-affinity transporter of inorganic phosphate, partially suppresses the αMG growth defect of an sgrS mutant. Induction of the stress response was also reduced in the sgrS pitA mutant compared to its sgrS parent. Microarray analysis suggested that expression of phosphate (Pho) regulon genes is increased in the sgrS pitA mutant compared to the sgrS parent. Consistent with this, we found increased PhoA (alkaline phosphatase) activity in the sgrS pitA mutant compared to the sgrS strain. Further, direct induction of the Pho regulon (in a pitA+ background) also resulted in partial suppression of the sgrS growth defect. The suppression was reversed when Pho induction was prevented by mutation of phoB, which encodes the Pho transcriptional activator. Deletion of individual Pho structural genes in suppressed strains did not identify a single gene responsible for suppression. Altogether, this work describes one of the first studies of glucose-phosphate stress physiology and suggests a novel connection of carbon and phosphate metabolism.

Original languageEnglish (US)
Pages (from-to)2520-2530
Number of pages11
JournalJournal of bacteriology
Volume194
Issue number10
DOIs
StatePublished - May 1 2012

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Regulon
Phosphates
Escherichia coli
Glucose
Growth
Phosphate Transport Proteins
Genes
Cell Physiological Phenomena
Glucose-6-Phosphate
Mutation
Facilitative Glucose Transport Proteins
Glucosides
Protein Biosynthesis
Microarray Analysis
Alkaline Phosphatase
Carbon
RNA
Bacteria

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

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title = "Induction of the Pho regulon suppresses the growth defect of an Escherichia coli sgrS mutant, connecting phosphate metabolism to the glucose-phosphate stress response",
abstract = "Some bacteria experience stress when glucose-6-phosphate or analogues like α-methyl glucoside-6-phosphate (αMG6P) accumulate in the cell. In Escherichia coli, the small SgrS RNA is vital to recovery from glucose-phosphate stress; the growth of sgrS mutants is strongly inhibited by αMG. SgrS helps to restore growth in part through inhibiting translation of the ptsG mRNA, which encodes the major glucose transporter EIICBGlc. While the regulatory mechanism of SgrS has been characterized, little is known about how glucose-phosphate stress connects to other aspects of cell physiology. In the present study, we discovered that mutation of pitA, which encodes the low-affinity transporter of inorganic phosphate, partially suppresses the αMG growth defect of an sgrS mutant. Induction of the stress response was also reduced in the sgrS pitA mutant compared to its sgrS parent. Microarray analysis suggested that expression of phosphate (Pho) regulon genes is increased in the sgrS pitA mutant compared to the sgrS parent. Consistent with this, we found increased PhoA (alkaline phosphatase) activity in the sgrS pitA mutant compared to the sgrS strain. Further, direct induction of the Pho regulon (in a pitA+ background) also resulted in partial suppression of the sgrS growth defect. The suppression was reversed when Pho induction was prevented by mutation of phoB, which encodes the Pho transcriptional activator. Deletion of individual Pho structural genes in suppressed strains did not identify a single gene responsible for suppression. Altogether, this work describes one of the first studies of glucose-phosphate stress physiology and suggests a novel connection of carbon and phosphate metabolism.",
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T1 - Induction of the Pho regulon suppresses the growth defect of an Escherichia coli sgrS mutant, connecting phosphate metabolism to the glucose-phosphate stress response

AU - Richards, Gregory R.

AU - Vanderpool, Carin K.

PY - 2012/5/1

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N2 - Some bacteria experience stress when glucose-6-phosphate or analogues like α-methyl glucoside-6-phosphate (αMG6P) accumulate in the cell. In Escherichia coli, the small SgrS RNA is vital to recovery from glucose-phosphate stress; the growth of sgrS mutants is strongly inhibited by αMG. SgrS helps to restore growth in part through inhibiting translation of the ptsG mRNA, which encodes the major glucose transporter EIICBGlc. While the regulatory mechanism of SgrS has been characterized, little is known about how glucose-phosphate stress connects to other aspects of cell physiology. In the present study, we discovered that mutation of pitA, which encodes the low-affinity transporter of inorganic phosphate, partially suppresses the αMG growth defect of an sgrS mutant. Induction of the stress response was also reduced in the sgrS pitA mutant compared to its sgrS parent. Microarray analysis suggested that expression of phosphate (Pho) regulon genes is increased in the sgrS pitA mutant compared to the sgrS parent. Consistent with this, we found increased PhoA (alkaline phosphatase) activity in the sgrS pitA mutant compared to the sgrS strain. Further, direct induction of the Pho regulon (in a pitA+ background) also resulted in partial suppression of the sgrS growth defect. The suppression was reversed when Pho induction was prevented by mutation of phoB, which encodes the Pho transcriptional activator. Deletion of individual Pho structural genes in suppressed strains did not identify a single gene responsible for suppression. Altogether, this work describes one of the first studies of glucose-phosphate stress physiology and suggests a novel connection of carbon and phosphate metabolism.

AB - Some bacteria experience stress when glucose-6-phosphate or analogues like α-methyl glucoside-6-phosphate (αMG6P) accumulate in the cell. In Escherichia coli, the small SgrS RNA is vital to recovery from glucose-phosphate stress; the growth of sgrS mutants is strongly inhibited by αMG. SgrS helps to restore growth in part through inhibiting translation of the ptsG mRNA, which encodes the major glucose transporter EIICBGlc. While the regulatory mechanism of SgrS has been characterized, little is known about how glucose-phosphate stress connects to other aspects of cell physiology. In the present study, we discovered that mutation of pitA, which encodes the low-affinity transporter of inorganic phosphate, partially suppresses the αMG growth defect of an sgrS mutant. Induction of the stress response was also reduced in the sgrS pitA mutant compared to its sgrS parent. Microarray analysis suggested that expression of phosphate (Pho) regulon genes is increased in the sgrS pitA mutant compared to the sgrS parent. Consistent with this, we found increased PhoA (alkaline phosphatase) activity in the sgrS pitA mutant compared to the sgrS strain. Further, direct induction of the Pho regulon (in a pitA+ background) also resulted in partial suppression of the sgrS growth defect. The suppression was reversed when Pho induction was prevented by mutation of phoB, which encodes the Pho transcriptional activator. Deletion of individual Pho structural genes in suppressed strains did not identify a single gene responsible for suppression. Altogether, this work describes one of the first studies of glucose-phosphate stress physiology and suggests a novel connection of carbon and phosphate metabolism.

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