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Iron-acquisition genes and siderophore production are induced by Salmonella Enteritidis in egg white at temperatures around the natural body temperature of hens

Abstract : Salmonella outbreaks are a serious threat to public health. One of the main vehicles of infection are eggs and egg-products, with Salmonella enterica serovar Enteritidis being the most frequent contaminant. Egg contamination occurs despite the impressive antibacterial properties of egg white and it is notable that S. Enteritidis is able to survive in egg white in contrast to other serovars and species. It is generally accepted that the major egg white-factor limiting growth of Salmonella is the highly iron-restricted environment resulting from the presence of ovotransferrin, an iron-binding protein. To circumvent iron restriction, many bacteria synthesise siderophores that can chelate iron from host iron-binding proteins for delivery to bacteria. The iron starvation response genes are regulated according to iron availability via the transcriptional regulator, Fur. Evidence for a relationship between temperature and iron sequestration ability has been reported by several groups. For Salmonella Typhymurium, little or no siderophore is secreted at 40-42°C in iron depleted medium indicating a temperature regulatory effect that is independent of Fur/Fe control. The aim of this study is to determine if egg white exposure induces the iron-acquisition genes and siderophore production in the highly-egg-white adapted Enteritidis serovar at ~40°C, the natural hen body temperature that Salmonella would encounter when infecting the egg during egg formation in the oviduct or during hatching. In order to easily recover of S. Enteritidis, we used egg white model medium (EWMM) in place of viscous egg white. EWMM consists of egg white filtrate with 10% egg white and numerous studies have validated this model medium. We measured the expression of 15 genes involved in the ironrestriction response by qRT-PCR after S. Enteritidis incubation of 45 minutes in EWMM at 37, 40 and 42°C. We observed a strong expression of genes encoding proteins involved in biosynthesis, export, uptake and utilisation of enterobactin and salmochelin (the two siderophores of Salmonella) and ferric-hydroxamate uptake. A statistical analysis shows that iron-acquisition genes are better expressed at 40°C than at 37 or 42°C. The production of siderophores was quantified during incubation using the Calcein blue test. Siderophores released by Salmonella in EWMM were detected at around a 1 μM desferral equivalent within 6h of incubation at 37, 40 and 42°C. The results of this study suggest that S. Enteritidis is able to induce its iron acquisition systems to cope with the iron-restricted conditions imposed by egg white even at the elevated body temperature of the hen.
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Conference papers
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https://hal.inrae.fr/hal-02737477
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Submitted on : Tuesday, June 2, 2020 - 7:22:58 PM
Last modification on : Thursday, March 18, 2021 - 11:44:09 AM

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  • HAL Id : hal-02737477, version 1
  • PRODINRA : 493719

Citation

Louis Julien, Kimon-Andreas Karatzas, Florence Baron, Marie-Françoise Cochet, Sylvie Bonnassie-Rouxin, et al.. Iron-acquisition genes and siderophore production are induced by Salmonella Enteritidis in egg white at temperatures around the natural body temperature of hens. International Symposium Salmonella and Salmonellosis (I3S), Sep 2018, Saint Malo, France. ⟨hal-02737477⟩

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