Salmonella Cold Stress Response: Mechanisms and Occurrence in Foods

Ricke, Steven C.; Dawoud, Turki M.; Kim, Sun Ae; Park, Si Hong; Kwon, Young Min

doi:10.1016/bs.aambs.2018.03.001

Cited by 41 publications

(17 citation statements)

References 175 publications

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“…CspA, the major and best-characterized cold shock protein, acts as a global regulator by binding to mRNA or single-stranded DNA. It can influence the transcriptional and translational properties of bacterial cells (42). For instance, Rennella et al highlighted the RNA binding and chaperone activity of CspA in E. coli (43).…”

Section: Resultsmentioning

confidence: 99%

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: 99%

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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“…To this aim, a total of 18 genes were selected for expression assessments based on their importance to the development of stress tolerance in S. Enteritidis. Briefly, we determined the expression profiles of two acid tolerance-related genes (SEN1564A and cfa) (Álvarez-Ordóñez et al, 2012;Joerger et al, 2012), four heat tolerance-related genes (rpoH, uspA, uspB, and htrA) (Yadav, Saxena, Saxena, & Kataria, 2016), five cold tolerance-related genes (cspA, cspC, cspD, cspE, and csdA) (Ricke, Dawoud, Kim, Park, & Kwon, 2018) and seven salt tolerancerelated genes (proP, proV, proW, proX, osmW, osmX, and osmY) (Frossard et al, 2012) in response to acid adaptation. Total RNA was extracted using Trizol reagent (Invitrogen, Carlsbad, CA, USA) according to the manufacturer's protocol.…”

Section: Reverse Transcription Quantitative Real-time Pcr (Rt-qpcr) Amentioning

confidence: 99%

Response to Acid Adaptation in Salmonella enterica Serovar Enteritidis

Zhou

et al. 2019

Journal of Food Science

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Acid adaptation in Salmonella Enteritidis was characterized by phenotypic and gene‐expression analyses. S. Enteritidis cells at log‐phase and stationary‐phase were kept at pH 4.5 to 6.0 for 1 to 4 hours. All treatments induced various levels of acid tolerance response that were dependent on pH, exposure time and growth phase. This acid adaptation resulted in tolerance to 50 °C and 8% NaCl regardless of the growth phase. However, the tolerance of log‐phase and stationary‐phase cells to low temperatures (4 and –20 °C) was increased and decreased, respectively. RT‐qPCR analysis revealed that genes involved in tolerance to acid (SEN1564A and cfa), heat (rpoH, uspB, and htrA), salt (proP, proV, and osmW), and cold (cspA, cspC, and csdA) stress were generally upregulated after acid adaptation. These results provide an initial insight into mechanisms of acid adaptation and induced cross protection in S. Enteritidis. Practical Application Stress tolerance acquisition resulting from acid adaptation in foodborne pathogens poses a great threat to food safety. The current work showed that acid adaptation induced direct tolerance and cross‐tolerance to high temperature, low temperature, and salt in Salmonella Enteritidis, possibly due to the upregulation of stress tolerance‐related genes. These results provide key insights into acid adaptation mechanisms and efficient control of S. Enteritidis.

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“…The similar roles of membrane fluidity have been demonstrated in cold and other stresses in many bacteria (Yoon et al, 2015;Eberlein et al, 2018). However, the fluidities are regulated by various mechanisms in different bacteria; e.g., E. coli (Carty et al, 1999), B. subtilis (Aguilar et al, 2001), and Salmonella (Wollenweber et al, 1983;Ricke et al, 2018).…”

Section: Cell Membrane and Fluidity At Low Temperaturementioning

confidence: 53%

Isolate Specific Cold Response of Yersinia enterocolitica in Transcriptional, Proteomic, and Membrane Physiological Changes

Murugaiyan

Thomas

et al. 2020

Front. Microbiol.

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Yersinia enterocolitica, a zoonotic foodborne pathogen, is able to withstand low temperatures. This psychrotrophic ability allows it to multiply in food stored in refrigerators. However, little is known about the Y. enterocolitica cold response. In this study, isolate-specific behavior at 4 • C was demonstrated and the cold response was investigated by examining changes in phenotype, gene expression, and the proteome. Altered expression of cold-responsive genes showed that the ability to survive at low temperature depends on the capacity to acclimate and adapt to cold stress. This cold acclimation at the transcriptional level involves the transient induction and effective repression of cold-shock protein (Csp) genes. Moreover, the resumption of expression of genes encoding other non-Csp is essential during prolonged adaptation. Based on proteomic analyses, the predominant functional categories of cold-responsive proteins are associated with protein synthesis, cell membrane structure, and cell motility. In addition, changes in membrane fluidity and motility were shown to be important in the cold response of Y. enterocolitica. Isolate-specific differences in the transcription of membrane fluidity-and motility-related genes provided evidence to classify strains within a spectrum of cold response. The combination of different approaches has permitted the systematic description of the Y. enterocolitica cold response and gives a better understanding of the physiological processes underlying this phenomenon.

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Salmonella Cold Stress Response: Mechanisms and Occurrence in Foods

Cited by 41 publications

References 175 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

Response to Acid Adaptation in Salmonella enterica Serovar Enteritidis

Isolate Specific Cold Response of Yersinia enterocolitica in Transcriptional, Proteomic, and Membrane Physiological Changes

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