Dataset Information

ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization.

ABSTRACT: OmpR is a multifunctional DNA binding regulator with orthologues in many enteric bacteria that exhibits classical regulator activity as well as nucleoid-associated protein-like characteristics. In the enteric pathogen Salmonella enterica, using chromatin immunoprecipitation of OmpR:FLAG and nucleotide sequencing, 43 putative OmpR binding sites were identified in S. enterica serovar Typhi, 22 of which were associated with OmpR-regulated genes. Mutation of a sequence motif (TGTWACAW) that was associated with the putative OmpR binding sites abrogated binding of OmpR:6×His to the tviA upstream region. A core set of 31 orthologous genes were found to exhibit OmpR-dependent expression in both S. Typhi and S. Typhimurium. S. Typhimurium-encoded orthologues of two divergently transcribed OmpR-regulated operons (SL1068-71 and SL1066-67) had a putative OmpR binding site in the inter-operon region in S. Typhi, and were characterized using in vitro and in vivo assays. These operons are widely distributed within S. enterica but absent from the closely related Escherichia coli. SL1066 and SL1067 were required for growth on N-acetylmuramic acid as a sole carbon source. SL1068-71 exhibited sequence similarity to sialic acid uptake systems and contributed to colonization of the ileum and caecum in the streptomycin-pretreated mouse model of colitis.

SUBMITTER: Perkins TT

PROVIDER: S-EPMC3586657 | biostudies-literature | 2013 Feb

REPOSITORIES: biostudies-literature

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ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization.

Perkins Timothy T TT Davies Mark R MR Klemm Elizabeth J EJ Rowley Gary G Wileman Thomas T James Keith K Keane Thomas T Maskell Duncan D Hinton Jay C D JC Dougan Gordon G Kingsley Robert A RA

Molecular microbiology 20121219 3

OmpR is a multifunctional DNA binding regulator with orthologues in many enteric bacteria that exhibits classical regulator activity as well as nucleoid-associated protein-like characteristics. In the enteric pathogen Salmonella enterica, using chromatin immunoprecipitation of OmpR:FLAG and nucleotide sequencing, 43 putative OmpR binding sites were identified in S. enterica serovar Typhi, 22 of which were associated with OmpR-regulated genes. Mutation of a sequence motif (TGTWACAW) that was asso ...[more]

PMID: 23190111

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Project description:Bacteria can coordinate behavior in response to population density through the production, release, and detection of small molecules, a phenomenon known as quorum sensing. Salmonella enterica is among a group of Enterobacteriaceae that can detect signaling molecules of the N-acyl homoserine lactone (AHL) type but lack the ability to produce them. The AHLs are detected by the LuxR-type transcription factor, SdiA. This enables a behavior known as eavesdropping, where organisms can sense the signaling molecules of other species of bacteria. The role of SdiA remains largely unknown. Here, we use RNA-seq to more completely identify the sdiA regulons of two clinically significant serovars of Salmonella enterica: Typhimurium and Typhi. We find that their sdiA regulons are largely conserved despite the significant differences in pathogenic strategy and host range of these two serovars. Previous studies identified sdiA-regulated genes in Escherichia coli and Enterobacter cloacae, but there is surprisingly no overlap in regulon membership between the different species. This led us to individually test orthologs of each regulon member in the other species and determine that there is indeed some overlap. Unfortunately, the functions of most sdiA-regulated genes are unknown, with the overall function of eavesdropping in these organisms remaining unclear.ImportanceMany bacterial species detect their own population density through the production, release, and detection of small molecules (quorum sensing). Salmonella and other Enterobacteriaceae have a modified system that detects the N-acyl-homoserine lactones of other bacteria through the solo quorum sensing receptor SdiA, a behavior known as eavesdropping. The roles of sdiA-dependent eavesdropping in the lifecycles of these bacteria are unknown. In this study, we identify sdiA-dependent transcriptional responses in two clinically relevant serovars of Salmonella, Typhimurium and Typhi, and note that their responses are partially conserved. We also demonstrate for the first time that sdiA-dependent regulation of genes is partially conserved in Enterobacter cloacae and Escherichia coli as well, indicating a degree of commonality in eavesdropping among the Enterobacteriaceae.

Project description:BackgroundSalmonella enterica subspecies I includes several closely related serovars which differ in host ranges and ability to cause disease. The basis for the diversity in host range and pathogenic potential of the serovars is not well understood, and it is not known how host-restricted variants appeared and what factors were lost or acquired during adaptations to a specific environment. Differences apparent from the genomic data do not necessarily correspond to functional proteins and more importantly differential regulation of otherwise identical gene content may play a role in the diverse phenotypes of the serovars of Salmonella.ResultsIn this study a comparative analysis of the cytosolic proteins of serovars Typhimurium and Pullorum was performed using two-dimensional gel electrophoresis and the proteins of interest were identified using mass spectrometry. An annotated reference map was created for serovar Typhimurium containing 233 entries, which included many metabolic enzymes, ribosomal proteins, chaperones and many other proteins characteristic for the growing cell. The comparative analysis of the two serovars revealed a high degree of variation amongst isolates obtained from different sources and, in some cases, the variation was greater between isolates of the same serovar than between isolates with different sero-specificity. However, several serovar-specific proteins, including intermediates in sulphate utilisation and cysteine synthesis, were also found despite the fact that the genes encoding those proteins are present in the genomes of both serovars.ConclusionCurrent microbial proteomics are generally based on the use of a single reference or type strain of a species. This study has shown the importance of incorporating a large number of strains of a species, as the diversity of the proteome in the microbial population appears to be significantly greater than expected. The characterisation of a diverse selection of strains revealed parts of the proteome of S. enterica that alter their expression while others remain stable and allowed for the identification of serovar-specific factors that have so far remained undetected by other methods.

Dataset Information

ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization.

Publications

ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization.

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