Functional Consequences of Genome Evolution inListeria monocytogenes: the lmo0423 and lmo0422 Genes Encode σ^Cand LstR, a Lineage II-Specific Heat Shock System

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 P SPAC 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.

Genome-wide transcriptional profiling of the cell envelope stress response and the role of LisRK and CesRK in Listeria monocytogenes

“…s M , s W and s X ), whereas in S. aureus, ECF s-factors are absent (Jordan et al, 2008). L. monocytogenes contains a single ECF s factor named s C (lmo0423), which has been shown to contribute to heat tolerance; however, no apparent link to the cell wall stress response has been observed (Zhang et al, 2005). The general stress sigma factor s B contributes to the tolerance of L. monocytogenes to cell-wall-acting antibiotics (Begley et al, 2006).…”

Whole-Genome Sequence ofListeria welshimeriReveals Common Steps in Genome Reduction withListeria innocuaas Compared toListeria monocytogenes

“…7. In addition, two gene clusters, one coding for a twin arginine secretion apparatus, TatAC (lmo0361-lmo0367), and the sigC gene cluster (lmo0421-lmo0423) (41), are lacking in the genome of L. welshimeri. It was previously reported that sigC codes for C , which is involved in thermal resistance specific for L. monocytogenes strains of phylogenetic lineage II (41).…”

“…In addition, two gene clusters, one coding for a twin arginine secretion apparatus, TatAC (lmo0361-lmo0367), and the sigC gene cluster (lmo0421-lmo0423) (41), are lacking in the genome of L. welshimeri. It was previously reported that sigC codes for C , which is involved in thermal resistance specific for L. monocytogenes strains of phylogenetic lineage II (41). When cultures of L. welshimeri, L. monocytogenes EGD-e, and L. innocua were assessed for survival following temperature upshift at 60°C for 0, 5, 10, and 15 min, only L. welshimeri was significantly impaired in its ability to recover from exposure to this nonpermissive temperature (see Fig.…”

Phenolic Acid-Mediated Regulation of the padC Gene, Encoding the Phenolic Acid Decarboxylase of Bacillus subtilis

“…However, AphA does not seem to be involved in phenolic acid metabolism in V. cholerae. More recently, the roles of two PadR-like repressors were reported for Listeria monocytogenes: LstR, which is required for effective thermal resistance (35), and LadR, the transcriptional regulator of the mdrL gene, which encodes a multidrug efflux transporter (15).…”