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Journal of Bacteriology, November 2005, p. 7243-7253, Vol. 187, No. 21
0021-9193/05/$08.00+0     doi:10.1128/JB.187.21.7243-7253.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Functional Consequences of Genome Evolution in Listeria monocytogenes: the lmo0423 and lmo0422 Genes Encode {sigma}C and LstR, a Lineage II-Specific Heat Shock System{dagger}

Chaomei Zhang, Joe Nietfeldt, Min Zhang, and Andrew K. Benson*

Department of Food Science and Technology, University of Nebraska, Lincoln, Nebraska 68583-0919

Received 28 June 2005/ Accepted 16 August 2005

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 lmo0422—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.

* Corresponding author. Mailing address: Department of Food Science and Technology, University of Nebraska, 330 Food Industry Complex, Lincoln, NE 68583-0919. Phone: (402) 472-5637. Fax: (402) 472-1693. E-mail: abenson1{at}unl.edu.

{dagger} A contribution of the University of Nebraska Agricultural Research Division, Lincoln (journal series no. 14675).

Journal of Bacteriology, November 2005, p. 7243-7253, Vol. 187, No. 21
0021-9193/05/$08.00+0     doi:10.1128/JB.187.21.7243-7253.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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