Identification of a regulator that controls stationary-phase expression of catalase-peroxidase in Caulobacter crescentus

Paul S. Rava, Laura Somma, Howard M. Steinman

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Expression of the catalase-peroxidase of Caulobacter crescentus, a gram- negative member of the α subdivision of the Proteobacteria, is 50-fold higher in stationary-phase cultures than in exponential cultures. To identify regulators of the starvation response, Tn5 insertion mutants were isolated with reduced expression of a katG::lacZ fusion on glucose starvation. One insertion interrupted an open reading frame encoding a protein with significant amino acid sequence identity to TipA, a helix-turn-helix transcriptional activator in the response of Streptomyces lividans to the peptide antibiotic thiostrepton, and lesser sequence similarity to other helix-turn-helix regulators in the MerR family. The C. crescentus orthologue of tipA was named skgA (stationary-phase regulation of katG). Stationary- phase expression of katG was reduced by 70% in the skgA::Tn5 mutant, and stationary-phase resistance to hydrogen peroxide decreased by a factor of 10. Like the wild type, the skgA mutant exhibited starvation-induced cross- resistance to heat and acid shock, entered into the helical morphology that occurs after 9 to 12 days in stationary phase, and during exponential growth induced katG in response to hydrogen peroxide challenge. Expression of skgA increased 5- to 10-fold in late exponential phase. skgA is the first regulator of a starvation-induced stress response identified in C. crescentus. SkgA is not a global regulator of the stationary-phase stress response; its action encompasses the oxidative stress-hydrogen peroxide response but not acid or heat responses. Moreover, SkgA is not an alternative σ factor, like RpoS, which controls multiple aspects of starvation-induced cross-resistance to stress in enteric bacteria. These observations raise the possibility that regulation of stationary-phase gene expression in this member of the α subdivision of the Proteobacteria is different from that in Escherichia coli and other members of the γ subdivision.

Original languageEnglish (US)
Pages (from-to)6152-6159
Number of pages8
JournalJournal of Bacteriology
Volume181
Issue number19
StatePublished - Oct 1999

Fingerprint

Caulobacter crescentus
Starvation
Catalase
Peroxidase
Hydrogen Peroxide
Proteobacteria
Thiostrepton
Hot Temperature
Streptomyces lividans
Acids
Enterobacteriaceae
Open Reading Frames
Amino Acid Sequence
Shock
Oxidative Stress
Escherichia coli
Anti-Bacterial Agents
Gene Expression
Glucose
Peptides

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Immunology

Cite this

Identification of a regulator that controls stationary-phase expression of catalase-peroxidase in Caulobacter crescentus. / Rava, Paul S.; Somma, Laura; Steinman, Howard M.

In: Journal of Bacteriology, Vol. 181, No. 19, 10.1999, p. 6152-6159.

Research output: Contribution to journalArticle

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abstract = "Expression of the catalase-peroxidase of Caulobacter crescentus, a gram- negative member of the α subdivision of the Proteobacteria, is 50-fold higher in stationary-phase cultures than in exponential cultures. To identify regulators of the starvation response, Tn5 insertion mutants were isolated with reduced expression of a katG::lacZ fusion on glucose starvation. One insertion interrupted an open reading frame encoding a protein with significant amino acid sequence identity to TipA, a helix-turn-helix transcriptional activator in the response of Streptomyces lividans to the peptide antibiotic thiostrepton, and lesser sequence similarity to other helix-turn-helix regulators in the MerR family. The C. crescentus orthologue of tipA was named skgA (stationary-phase regulation of katG). Stationary- phase expression of katG was reduced by 70{\%} in the skgA::Tn5 mutant, and stationary-phase resistance to hydrogen peroxide decreased by a factor of 10. Like the wild type, the skgA mutant exhibited starvation-induced cross- resistance to heat and acid shock, entered into the helical morphology that occurs after 9 to 12 days in stationary phase, and during exponential growth induced katG in response to hydrogen peroxide challenge. Expression of skgA increased 5- to 10-fold in late exponential phase. skgA is the first regulator of a starvation-induced stress response identified in C. crescentus. SkgA is not a global regulator of the stationary-phase stress response; its action encompasses the oxidative stress-hydrogen peroxide response but not acid or heat responses. Moreover, SkgA is not an alternative σ factor, like RpoS, which controls multiple aspects of starvation-induced cross-resistance to stress in enteric bacteria. These observations raise the possibility that regulation of stationary-phase gene expression in this member of the α subdivision of the Proteobacteria is different from that in Escherichia coli and other members of the γ subdivision.",
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