Quantitative proteomics reveals the crucial role of YbgC for Salmonella enterica serovar Enteritidis survival in egg white

Qin, Xiaojie; He, Shoukui; Zhou, Xiujuan; Cheng, Xu; Huang, Xiaozhen; Wang, Yanyan; Wang, Siyun; Cui, Yan; Shi, Chunlei; Shi, Xianming

doi:10.1016/j.ijfoodmicro.2018.08.010

Cited by 24 publications

(22 citation statements)

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“…It should be noted that differential proteins with moderate iTRAQ ratios may also be important to bacterial stress responses. For example, YbgC was upregulated by 1.20-and 1.46-fold, as identified by the iTRAQ experiments, after the exposure of S. Enteritidis to 50% and 80% egg white, respectively; mutagenic analysis further revealed that YbgC was indeed a key protein contributing to S. Enteritidis survival in egg white (16). Therefore, all significantly differentially expressed proteins, including those with moderate iTRAQ ratios, were utilized to uncover ethanol adaptation mechanisms in S. Enteritidis in the current study.…”

Section: Resultsmentioning

confidence: 91%

“…In fact, there is increasing evidence implicating the role of enterobactin in bacterial stress responses. For example, enterobactin biosynthesis and uptake were induced following exposure of S. Enteritidis to egg white to facilitate iron acquisition, thus providing a survival advantage to this bacterium (16,49). Peralta et al found that enterobactin protected E. coli against oxidative stress and that this effect was independent of its capacity to scavenge iron (50).…”

Section: Resultsmentioning

confidence: 99%

“…Nonadapted and ethanol-adapted cells of S. Enteritidis were washed twice with PBS, resuspended in SDT buffer (1 mM dithiothreitol [DTT], 4% SDS, and 150 mM Tris-HCl [pH 8.0]), boiled for 5 min, and ultrasonicated for another 5 min. The lysates were centrifuged at 14,000 ϫ g for 10 min to remove cellular debris (16). The resulting supernatants were transferred to new tubes and stored at Ϫ80°C for subsequent use.…”

Section: Methodsmentioning

confidence: 99%

“…Additionally, quantitative proteomics revealed the important role of YbgC in the survival of Salmonella enterica subsp. enterica serovar Enteritidis in egg white (16). It is therefore expected that this technology will be helpful to provide an insight into the molecular and cellular bases of ethanol adaptation in foodborne pathogens.…”

mentioning

confidence: 99%

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Ethanol Adaptation Strategies in Salmonella enterica Serovar Enteritidis Revealed by Global Proteomic and Mutagenic Analyses

Qin

Wong

et al. 2019

Appl Environ Microbiol

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Salmonella enterica subsp. enterica serovar Enteritidis is able to adapt to sublethal concentrations of ethanol, which subsequently induce tolerance of this pathogen to normally lethal ethanol challenges. This work aims to elucidate the underlying ethanol adaptation mechanisms of S. Enteritidis by proteomic and mutagenic analyses. The global proteomic response of S. Enteritidis to ethanol adaptation (5% ethanol for 1 h) was determined by isobaric tags for relative and absolute quantification (iTRAQ), and it was found that a total of 138 proteins were differentially expressed in ethanol-adapted cells compared to nonadapted cells. A total of 56 upregulated proteins were principally associated with purine metabolism and as transporters for glycine betaine, phosphate, d-alanine, thiamine, and heme, whereas 82 downregulated proteins were mainly involved in enterobactin biosynthesis and uptake, the ribosome, flagellar assembly, and virulence. Moreover, mutagenic analysis further revealed the functions of two highly upregulated proteins belonging to purine metabolism (HiuH, 5-hydroxyisourate hydrolase) and glycine betaine transport (ProX, glycine betaine-binding periplasmic protein) pathways. Deletion of either hiuH or proX resulted in the development of a stronger ethanol tolerance response, suggesting negative regulatory roles in ethanol adaptation. Collectively, this work suggests that S. Enteritidis employs multiple strategies to coordinate ethanol adaptation. IMPORTANCE Stress adaptation in foodborne pathogens has been recognized as a food safety concern since it may compromise currently employed microbial intervention strategies. While adaptation to sublethal levels of ethanol is able to induce ethanol tolerance in foodborne pathogens, the molecular mechanism underlying this phenomenon is poorly characterized. Hence, global proteomic analysis and mutagenic analysis were conducted in the current work to understand the strategies employed by Salmonella enterica subsp. enterica serovar Enteritidis to respond to ethanol adaptation. It was revealed that coordinated regulation of multiple pathways involving metabolism, ABC transporters, regulators, enterobactin biosynthesis and uptake, the ribosome, flagellar assembly, and virulence was responsible for the development of ethanol adaptation response in this pathogen. Such knowledge will undoubtedly contribute to the development and implementation of more-effective food safety interventions.

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Section: Resultsmentioning

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Ethanol Adaptation Strategies in Salmonella enterica Serovar Enteritidis Revealed by Global Proteomic and Mutagenic Analyses

Qin

Wong

et al. 2019

Appl Environ Microbiol

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“…A recent global transcriptomic study (Baron et al 2017 ) revealed a major iron-starvation response of S E upon exposure to egg white which was caused by relief of Fur- (the global transcriptional regulator of iron-dependent gene expression; Rabsch et al 2003 ) mediated repression. Likewise, a quantitative proteomic analysis (isobaric tags for relative and absolute quantitation; iTRAQ) showed that iron-acquisition-system-related proteins are induced by egg white (Qin et al 2019 ). These findings confirm that S E suffers from iron limitation in egg white.…”

Section: Survival Of Salmonella Within Egg White Amentioning

confidence: 99%

The anti-bacterial iron-restriction defence mechanisms of egg white; the potential role of three lipocalin-like proteins in resistance against Salmonella

et al. 2019

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Salmonella enterica serovar Enteritidis ( S E) is the most frequently-detected Salmonella in foodborne outbreaks in the European Union. Among such outbreaks, egg and egg products were identified as the most common vehicles of infection. Possibly, the major antibacterial property of egg white is iron restriction, which results from the presence of the iron-binding protein, ovotransferrin. To circumvent iron restriction, S E synthesise catecholate siderophores (i.e. enterobactin and salmochelin) that can chelate iron from host iron-binding proteins. Here, we highlight the role of lipocalin-like proteins found in egg white that could enhance egg-white iron restriction through sequestration of certain siderophores, including enterobactin. Indeed, it is now apparent that the egg-white lipocalin, Ex-FABP, can inhibit bacterial growth via its siderophore-binding capacity in vitro. However, it remains unclear whether Ex-FABP performs such a function in egg white or during bird infection. Regarding the two other lipocalins of egg white (Cal-γ and α-1-glycoprotein), there is currently no evidence to indicate that they sequester siderophores.

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Proteomic analysis of the antimicrobial effects of sublethal concentrations of thymol on Salmonella enterica serovar Typhimurium

Zhao

Wang

Pei

et al. 2020

Appl Microbiol Biotechnol

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Quantitative proteomics reveals the crucial role of YbgC for Salmonella enterica serovar Enteritidis survival in egg white

Cited by 24 publications

References 50 publications

Ethanol Adaptation Strategies in Salmonella enterica Serovar Enteritidis Revealed by Global Proteomic and Mutagenic Analyses

Ethanol Adaptation Strategies in Salmonella enterica Serovar Enteritidis Revealed by Global Proteomic and Mutagenic Analyses

The anti-bacterial iron-restriction defence mechanisms of egg white; the potential role of three lipocalin-like proteins in resistance against Salmonella

Proteomic analysis of the antimicrobial effects of sublethal concentrations of thymol on Salmonella enterica serovar Typhimurium

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