Functional consequences of genome evolution in Listeria monocytogenes

The lmo0423 and lmo0422 genes encode σC and LstR, a lineage II-specific heat shock system

Chaomei Zhang, Joe Nietfeldt, Min Zhang, Andrew K Benson

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

Listeria monocytogenes strains belonging to phylogenetic lineage II (serotypes 1/2a, 1/2c, and 3a) carry a lineage-specific genome segment encoding a putative sigma subunit of RNA polymerase (lmo0423, herein referred to as sigC), a gene of unknown function (lmo0422) similar to the padR family of regulators, and a gene that is similar to the rodA-ftsW family of cell wall morphology genes (lmo0421). To understand the function of this set of genes, their expression patterns and the effects of null mutations in the lineage II L. monocytogenes strain 10403S were examined. The data are consistent with the three genes comprising an operon (the sigC operon) that is highly induced by temperature upshift. The operon is transcribed from three different promoters, the proximal of which (P1) depends upon sigC itself. Null mutations in sigC or lmo0422 increase the death rate at lethal temperatures and cause loss of thermal adaptive response, whereas the lmo0421 mutation causes only a loss of the adaptive response component. Only the sigC mutation affects transcription from the P1 promoter, whereas ectopic expression of lmo0422 from the PSPAC promoter complements the individual lmo0422 and sigC null mutations, showing that lmo0422 is the actual thermal resistance regulator or effector while sigC provides a mechanism for temperature-dependent transcription of lmo0422 from P1. Our genetic and phylogenetic analyses are consistent with 1mo0422-renamed lstR (for lineage-specific thermal regulator)-and sigC comprising a system of thermal resistance that was ancestral to the genus Listeria and was subsequently lost during divergence of the lineage I L. monocytogenes population.

Original languageEnglish (US)
Pages (from-to)7243-7253
Number of pages11
JournalJournal of bacteriology
Volume187
Issue number21
DOIs
StatePublished - Nov 1 2005

Fingerprint

Listeria monocytogenes
Shock
Hot Temperature
Genome
Operon
Mutation
Genes
Temperature
Sigma Factor
Listeria
DNA-Directed RNA Polymerases
Regulator Genes
Cell Wall
Gene Expression
Mortality
Population

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Functional consequences of genome evolution in Listeria monocytogenes : The lmo0423 and lmo0422 genes encode σC and LstR, a lineage II-specific heat shock system. / Zhang, Chaomei; Nietfeldt, Joe; Zhang, Min; Benson, Andrew K.

In: Journal of bacteriology, Vol. 187, No. 21, 01.11.2005, p. 7243-7253.

Research output: Contribution to journalArticle

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abstract = "Listeria monocytogenes strains belonging to phylogenetic lineage II (serotypes 1/2a, 1/2c, and 3a) carry a lineage-specific genome segment encoding a putative sigma subunit of RNA polymerase (lmo0423, herein referred to as sigC), a gene of unknown function (lmo0422) similar to the padR family of regulators, and a gene that is similar to the rodA-ftsW family of cell wall morphology genes (lmo0421). To understand the function of this set of genes, their expression patterns and the effects of null mutations in the lineage II L. monocytogenes strain 10403S were examined. The data are consistent with the three genes comprising an operon (the sigC operon) that is highly induced by temperature upshift. The operon is transcribed from three different promoters, the proximal of which (P1) depends upon sigC itself. Null mutations in sigC or lmo0422 increase the death rate at lethal temperatures and cause loss of thermal adaptive response, whereas the lmo0421 mutation causes only a loss of the adaptive response component. Only the sigC mutation affects transcription from the P1 promoter, whereas ectopic expression of lmo0422 from the PSPAC promoter complements the individual lmo0422 and sigC null mutations, showing that lmo0422 is the actual thermal resistance regulator or effector while sigC provides a mechanism for temperature-dependent transcription of lmo0422 from P1. Our genetic and phylogenetic analyses are consistent with 1mo0422-renamed lstR (for lineage-specific thermal regulator)-and sigC comprising a system of thermal resistance that was ancestral to the genus Listeria and was subsequently lost during divergence of the lineage I L. monocytogenes population.",
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