Dataset Information

Acquisition of Iron Is Required for Growth of Salmonella spp. in Tomato Fruit.

ABSTRACT: Salmonella remains a leading cause of bacterial food-borne disease, sickening millions each year. Although outbreaks of salmonellosis have traditionally been associated with contaminated meat products, recent years have seen numerous disease cases caused by the consumption of produce. Tomatoes have been specifically implicated, due to the ability of Salmonella spp. to enter the tomato fruit and proliferate within, making the decontamination of the raw product impossible. To investigate the genetic means by which Salmonella is able to survive and proliferate within tomatoes, we conducted a screen for bacterial genes of Salmonella enterica serovar Montevideo specifically induced after inoculation into ripe tomato fruit. Among these genes, we found 17 members of the previously described anaerobic Fur (ferric uptake regulator) regulon. Fur is a transcriptional and posttranscriptional regulator known to sense iron, suggesting the importance of this mineral to Salmonella within tomatoes. To test whether iron acquisition is essential for Salmonella growth in tomatoes, we tested a ?fepDGC mutant, which lacks the ability to import iron-associated siderophores. This mutant grew significantly more poorly within tomatoes than did the wild type, but the growth defect of the mutant was fully reversed by the addition of exogenous iron, demonstrating the need for bacterial iron scavenging. Further, dependence upon iron was not apparent for Salmonella growing in filtered tomato juice, implicating the cellular fraction of the fruit as an important mediator of iron acquisition by the bacteria.

SUBMITTER: Nugent SL

PROVIDER: S-EPMC4421055 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Acquisition of Iron Is Required for Growth of Salmonella spp. in Tomato Fruit.

Nugent Staci L SL Meng Fanhong F Martin Gregory B GB Altier Craig C

Applied and environmental microbiology 20150320 11

Salmonella remains a leading cause of bacterial food-borne disease, sickening millions each year. Although outbreaks of salmonellosis have traditionally been associated with contaminated meat products, recent years have seen numerous disease cases caused by the consumption of produce. Tomatoes have been specifically implicated, due to the ability of Salmonella spp. to enter the tomato fruit and proliferate within, making the decontamination of the raw product impossible. To investigate the genet ...[more]

PMID: 25795672

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Project description:Iron limitation is a universal strategy of host immunity during bacterial infection. However, the mechanisms by which pathogens antagonize host nutritional immunity have not been fully elucidated. Here, we identified a requirement for the UMPylator YdiU for this process in Salmonella. The expression of YdiU was dramatically induced by the metal starvation signal. The intracellular iron content was much lower in the ΔydiU strain than in wild-type Salmonella, and the ΔydiU strain exhibited severe growth defect under metal deficiency environments. Genome-wide expression analyses revealed significantly decreased expression of iron uptake genes in ΔydiU strain compared with the wild-type strain. Interestingly, YdiU did not affect the expression level of the major iron uptake regulator Fur but directly UMPylated Fur on its H118 residue in vivo and in vitro. UMPylation destroyed the Fur dimer, promoted Fur aggregation, and eliminated the DNA-binding activity of Fur, thus abolishing the ability of Fur to inhibit iron uptake. Restricting Fur to the deUMPylated state dramatically eliminates Salmonella iron uptake in iron deficiency environments. In parallel, YdiU facilitates Salmonella survival within host cells by regulating the iron uptake pathway. IMPORTANCE Salmonella is the major pathogen causing bacterial enteric illness in both humans and animals. Iron availability is strictly controlled upon Salmonella entry into host cells. The mechanisms by which Salmonella balances the acquisition of sufficient iron while preventing a toxic overload has not been fully understood. Here, we reveal a novel regulation process of iron acquisition mediated by the UMPylator YdiU. Fur acts as the central regulator of bacterial iron homeostasis. YdiU UMPylates Fur on H118 and prevents Fur from binding to target DNA, thus activating the expression of iron uptake genes under iron-deficient conditions. We describe the first posttranslational modification-based regulation of Fur and highlight a potential mechanism by which Salmonella can adapt to eliminate host nutritional immunity.

Dataset Information

Acquisition of Iron Is Required for Growth of Salmonella spp. in Tomato Fruit.

Publications

Acquisition of Iron Is Required for Growth of Salmonella spp. in Tomato Fruit.

Similar Datasets

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