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Complementation of Listeria monocytogenes null mutants with selected Listeria seeligeri virulence genes suggests functional adaptation of Hly and PrfA and considerable diversification of prfA regulation in L. seeligeri.

ABSTRACT: While Listeria seeligeri and L. monocytogenes contain the main Listeria virulence gene cluster, only L. monocytogenes is considered an intracellular pathogen. Initial evolutionary analyses showed that the virulence genes prfA, hly, and plcA are conserved in L. seeligeri, with specific Hly and PrfA amino acid residues showing evidence for positive selection in L. seeligeri. Our data also show that temperature-dependent transcript patterns for prfA, which encodes a transcriptional regulator of virulence genes, differed between L. monocytogenes and L. seeligeri. To further investigate the divergence of virulence gene function and regulation, L. seeligeri prfA (prfA(LS)), hly (hly(LS)), and plcA (plcA(LS)), as well as prfA(LS) constructs with different prfA promoter regions, were introduced into appropriate L. monocytogenes null mutants. Only when prfA(LS) was under the control of the L. monocytogenes prfA promoters (P1- and P2prfA) (P1P2(LM) prfA(LS)) was prfA(LS) able to fully complement the Delta prfA(LM) deletion. hly(LS) introduced into an L. monocytogenes background under its native promoter showed transcript levels similar to those of hly(LM) and was able to partially restore L. monocytogenes wild-type-level hemolysis and intracellular growth, even though Hly(LM) and Hly(LS) showed distinct patterns of cell- and supernatant-associated hemolytic activities. Our data indicate that (i) regulation of prfA expression differs between L. monocytogenes and L. seeligeri, although hly transcription is temperature dependent in both species, and (ii) PrfA and Hly functions are largely, but not fully, conserved between L. seeligeri and L. monocytogenes. Virulence gene homologues and their expression thus appear to have adapted to distinct but possibly related functions in these two species.

SUBMITTER: Stelling CR

PROVIDER: S-EPMC2916458 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Complementation of Listeria monocytogenes null mutants with selected Listeria seeligeri virulence genes suggests functional adaptation of Hly and PrfA and considerable diversification of prfA regulation in L. seeligeri.

Stelling Courtney R Lucas CR Orsi Renato H RH Wiedmann Martin M

Applied and environmental microbiology 20100611 15

While Listeria seeligeri and L. monocytogenes contain the main Listeria virulence gene cluster, only L. monocytogenes is considered an intracellular pathogen. Initial evolutionary analyses showed that the virulence genes prfA, hly, and plcA are conserved in L. seeligeri, with specific Hly and PrfA amino acid residues showing evidence for positive selection in L. seeligeri. Our data also show that temperature-dependent transcript patterns for prfA, which encodes a transcriptional regulator of vir ...[more]

PMID: 20543041

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Project description:Listeria monocytogenes is able to efficiently utilize glycerol as a carbon source. In a defined minimal medium, the growth rate (during balanced growth) in the presence of glycerol is similar to that in the presence of glucose or cellobiose. Comparative transcriptome analyses of L. monocytogenes showed high-level transcriptional upregulation of the genes known to be involved in glycerol uptake and metabolism (glpFK and glpD) in the presence of glycerol (compared to that in the presence of glucose and/or cellobiose). Levels of expression of the genes encoding a second putative glycerol uptake facilitator (GlpF(2)) and a second putative glycerol kinase (GlpK(2)) were less enhanced under these conditions. GlpK(1) but not GlpK(2) was essential for glycerol catabolism in L. monocytogenes under extracellular conditions, while the loss of GlpK(1) affected replication in Caco-2 cells less than did the loss of GlpK(2) and GlpD. Additional genes whose transcription levels were higher in the presence of glycerol than in the presence of glucose and cellobiose included those for two dihydroxyacetone (Dha) kinases and many genes that are under carbon catabolite repression control. Transcriptional downregulation in the presence of glycerol (compared to those in the presence glucose and cellobiose) was observed for several genes and operons that are positively regulated by glucose, including genes involved in glycolysis, N metabolism, and the biosynthesis of branched-chain amino acids. The highest level of transcriptional upregulation was observed for all PrfA-dependent genes during early and late logarithmic growth in glycerol. Under these conditions, a low level of HPr-Ser-P and a high level of HPr-His-P were present in the cells, suggesting that all enzyme IIA (EIIA) (or EIIB) components of the phosphotransferase system (PTS) permeases expressed will be phosphorylated. These and other data suggest that the phosphorylation state of PTS permeases correlates with PrfA activity.

Dataset Information

Complementation of Listeria monocytogenes null mutants with selected Listeria seeligeri virulence genes suggests functional adaptation of Hly and PrfA and considerable diversification of prfA regulation in L. seeligeri.

Publications

Complementation of Listeria monocytogenes null mutants with selected Listeria seeligeri virulence genes suggests functional adaptation of Hly and PrfA and considerable diversification of prfA regulation in L. seeligeri.

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