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Transcriptomic response of Listeria monocytogenes to iron limitation and Fur mutation.

ABSTRACT: Iron is required by almost all bacteria, but concentrations above physiological levels are toxic. In bacteria, intracellular iron is regulated mostly by the ferric uptake regulator, Fur, or a similar functional protein. Iron limitation results in the regulation of a number of genes, especially those involved in iron uptake. A subset of these genes is the Fur regulon under the control of Fur. In the present study, we have identified Fur- and iron-regulated genes in Listeria monocytogenes by DNA microarray analysis using a fur mutant and its isogenic parent. To identify genes regulated exclusively in response to iron limitation, the whole-genome transcriptional responses to the iron limitation of a fur mutant and its isogenic parent were compared. Fur-regulated genes were identified by comparing the transcriptional profile of the parent with the transcriptional profile of the isogenic fur mutant. Our studies have identified genes regulated exclusively in response to iron and those that are negatively regulated by Fur. We have identified at least 14 genes that were negatively regulated directly by Fur. Under iron-limited conditions, these genes were upregulated, while the expression of fur was found to be downregulated. To further investigate the regulation of fur in response to iron, an ectopic fur promoter-lacZ transcriptional fusion strain was constructed, and its isogenic fur and perR mutant derivatives were generated in L. monocytogenes 10403S. Analysis of the iron limitation of the perR mutant indicated that the regulation of genes under the negative control of Fur was significantly inhibited. Our results indicate that Fur and PerR proteins negatively regulate fur and that under iron-limited conditions, PerR is required for the negative regulation of genes controlled by Fur.

SUBMITTER: Ledala N

PROVIDER: S-EPMC2805226 | biostudies-literature | 2010 Jan

REPOSITORIES: biostudies-literature

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Transcriptomic response of Listeria monocytogenes to iron limitation and Fur mutation.

Ledala Nagender N Sengupta Mrittika M Muthaiyan Arunachalam A Wilkinson Brian J BJ Jayaswal R K RK

Applied and environmental microbiology 20091120 2

Iron is required by almost all bacteria, but concentrations above physiological levels are toxic. In bacteria, intracellular iron is regulated mostly by the ferric uptake regulator, Fur, or a similar functional protein. Iron limitation results in the regulation of a number of genes, especially those involved in iron uptake. A subset of these genes is the Fur regulon under the control of Fur. In the present study, we have identified Fur- and iron-regulated genes in Listeria monocytogenes by DNA m ...[more]

PMID: 19933349

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Project description:A long-term-survival (LTS) phase in Listeria monocytogenes was recently discovered. Cells in this phase are coccoid in shape, survive for at least 30 d without any decrease in viable cell numbers, and are very resistant to heat and high pressure. However, how cells of L. monocytogenes transition to this long-term-survival phase is little understood. Therefore, a whole-genome expression analysis was conducted to study the transcription profile of L. monocytogenes as it enters the LTS phase. Transcription profiles at log, stationary and death phases were analyzed since differential gene expressions at these phases may contribute to the eventual transition to the LTS phase. Specifically, cells of L. monocytogenes F2365 at log, stationary, death and LTS phases were obtained by incubating cultures in TSBYE at 35°C for 13 h, 17 h, 24 h and 168-336 h, respectively. Also, to study cells transitioning from the LTS phase back to the log phase, 1 ml of the LTS-phase culture at 336 h was reinoculated into 100 ml of fresh TSBYE with incubation at 35°C for 8 h. Total RNAs of all samples were extracted, reverse transcribed into cDNAs and then hybridized to the L. monocytogenes expression microarray (Roche NimbleGen). During the transition from log phase to stationary phase, differential changes in gene expression involved genes associated with cell envelope, cell division, stress response, energy metabolism, protein synthesis and material transport. During the transition from stationary to death phase, differential changes were observed in genes related to cell envelope, detoxification, pathogenesis, energy metabolism, protein synthesis and material transport. When cultures transitioned from death phase to 168-h LTS phase, significant downregulation of genes associated with amino acid and protein biosynthesis, as well as stress responses, were observed (P < 0.05), while multiple genes related to cell envelope, energy production and material transportation were significantly upregulated (P < 0.05). High similarity of transcription profiles (r = 0.93) within LTS phase was observed when comparing transcriptomes at 168 h and 336 h. RNA quality measurement revealed a high level of degradation of ribosomal RNA during the LTS phase. The transcription profile at 8-h (log-phase) after re-inoculation of LTS cells also resembled that at 13 h (r = 0.94). We hypothesize that the upregulation of some compatible solute transporters during the LTS phase may result in accumulation of these solutes, which may lower intracellular water activity and thus enhance resistance of L. monocytogenes to heat and high pressure. Dormancy may be induced at the LTS phase which is suggested by the downregulation of genes associated with transcription and translation. Once fresh nutrients are provided, LTS cells may quickly exit dormancy and become metabolically active as they transition to the log phase.

Dataset Information

Transcriptomic response of Listeria monocytogenes to iron limitation and Fur mutation.

Publications

Transcriptomic response of Listeria monocytogenes to iron limitation and Fur mutation.

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