Survival characteristics of <i>Salmonella enterica</i> serovar Enteritidis in chicken egg albumen

Kang, Hyun Wol; Loui, Cindy; Clavijo, Raul I.; Riley, Lee W.; Lu, Sangwei

doi:10.1017/s0950268806006054

Cited by 59 publications

(83 citation statements)

References 36 publications

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“…Biofilm formation is important for the survival of Salmonella on surfaces, for increased resistance to disinfectants, and for survival in the avian reproductive tract (112,113). Several genes in the S. Enteritidis genome provide this bacterium a unique ability to infect reproductive organs of chickens and contaminate forming eggs (114)(115)(116)(117). Two genes (wrbA and yshA) with possible involvement in biofilm formation (112, 118) and two genes (ygdl and SEN2997) that were previously implicated in the survival of S. Enteritidis in egg albumen (115) showed significantly reduced expression in LP strains.…”

Section: Resultsmentioning

confidence: 99%

RNA Sequencing Reveals Differences between the Global Transcriptomes of Salmonella enterica Serovar Enteritidis Strains with High and Low Pathogenicities

Shah

2014

Appl Environ Microbiol

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Salmonella enterica serovar Enteritidis is one of the important causes of bacterial food-borne gastroenteritis worldwide. Field strains of S. Enteritidis are relatively genetically homogeneous; however, they show extensive phenotypic diversity and differences in virulence potential. RNA sequencing (RNA-Seq) was used to characterize differences in the global transcriptome between several genetically similar but phenotypically diverse poultry-associated field strains of S. Enteritidis grown in laboratory medium at avian body temperature (42°C). These S. Enteritidis strains were previously characterized as high-pathogenicity (HP; n ‫؍‬ 3) and low-pathogenicity (LP; n ‫؍‬ 3) strains based on both in vitro and in vivo virulence assays. Using the negative binomial distribution-based statistical tools edgeR and DESeq, 252 genes were identified as differentially expressed in LP strains compared with their expression in the HP strains (P < 0.05). A majority of genes (235, or 93.2%) showed significantly reduced expression, whereas a few genes (17, or 6.8%) showed increased expression in all LP strains compared with HP strains. LP strains showed a unique transcriptional profile that is characterized by significantly reduced expression of several transcriptional regulators and reduced expression of genes involved in virulence (e.g., Salmonella pathogenicity island 1 [SPI-1], SPI-5, and fimbrial and motility genes) and protection against osmotic, oxidative, and other stresses, such as iron-limiting conditions commonly encountered within the host. Several functionally uncharacterized genes also showed reduced expression. This study provides a first concise view of the global transcriptional differences between field strains of S. Enteritidis with various levels of pathogenicity, providing the basis for future functional characterization of several genes with potential roles in virulence or stress regulation of S. Enteritidis.

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Section: Resultsmentioning

confidence: 99%

RNA Sequencing Reveals Differences between the Global Transcriptomes of Salmonella enterica Serovar Enteritidis Strains with High and Low Pathogenicities

Shah

2014

Appl Environ Microbiol

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“…One of them, isolate 47/03, lacks rpoS that codes for the stress-induced sigma factor and SEN4286, a gene involved in a type I restriction modification system (5), two features that may explain its deficiency in survival under these conditions of stress. Isolate 31/88 lacks genes coding for cytochrome C synthesis, ferredoxin, alcohol dehydrogenase, aldehyde dehydrogenase, and ethanolamine utilization (5), which could explain its survival-deficient phenotype (25). Isolate 254/01 was indistinguishable from PT4 genomically (5), suggesting that other underlying factors not detected in our CGH analysis may cause the difference in survival.…”

Section: Survival Of S Enteritidis Isolates In Egg Albumenmentioning

confidence: 99%

“…Egg albumen can repress the proliferation of S. Enteritidis due to iron restriction, high pH, and enzymatic activities that destabilize the bacterial cell wall (25). It is postulated that survival in egg albumen is essential for S. Enteritidis transmission to humans (21).…”

Section: Survival Of S Enteritidis Isolates In Egg Albumenmentioning

confidence: 99%

Differential Phenotypic Diversity among Epidemic-Spanning Salmonella enterica Serovar Enteritidis Isolates from Humans or Animals

Yim

Betancor

Martinez

et al. 2010

Appl Environ Microbiol

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Nontyphoidal salmonellae are major causes of food-borne disease worldwide. In Uruguay, Salmonella enterica serovar Enteritidis was the most commonly isolated serovar throughout the last decade, with a marked epidemic period between 1995 and 2004. In a previous study, we conducted comparative genomics of 29 epidemic-spanning S. Enteritidis field isolates, and here we evaluated the pathogenic potential of the same set of isolates using several phenotypic assays. The sample included 15 isolates from human gastroenteritis, 5 from invasive disease, and 9 from nonhuman sources. Contrary to the genetic homogeneity previously observed, we found great phenotypic variability among these isolates. One-third of them were defective in at least one assay, namely, 10 isolates were defective in motility, 8 in invasion of Caco-2 cells, and 10 in survival in egg albumen. Twelve isolates were tested for invasiveness in 3-day-old chickens, and five of these were significantly less invasive than the reference strain. The two oldest preepidemic isolates were reduced in fitness in all assays, providing a plausible explanation for the previous negligible incidence of S. Enteritidis in Uruguay and supporting the view that the introduction or emergence of a more virulent strain was responsible for the marked rise of this serovar. Further, we found differences in fitness among the isolates which depended on the source of isolation.

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“…For instance, the two major avian innate defenses that impose severe stress on an invading Salmonella Enteritidis include the acidic stress from gastric acidity (pH 2.6) ( Joyner and Kokas, 1971;Carter and Collins, 1974) and oxidative stress from effects of hydrogen peroxide (H 2 O 2 ) produced by infected avian heterophils and macrophages (Qureshi et al, 2000;Withanage et al, 2005;Kogut et al, 2002). Furthermore, egg albumen contains several antibacterial substances such as lysozyme, ovatransferrin, and avian Bdefensins (Van Immerseel, 2010;Kang et al, 2006), thereby presenting another detrimental environment for the survival and growth of this bacterium. Assessing the ability of Salmonella Enteritidis strains to survive under different stress conditions encountered early during infection in chickens may facilitate better understanding of the pathogenesis of Salmonella Enteritidis.…”

Section: Introductionmentioning

confidence: 99%

SalmonellaEnteritidis Strains from Poultry Exhibit Differential Responses to Acid Stress, Oxidative Stress, and Survival in the Egg Albumen

Shah

Casavant

Hawley

et al. 2012

Foodborne Pathogens and Disease

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Salmonella Enteritidis is the major foodborne pathogen that is primarily transmitted by contaminated chicken meat and eggs. We recently demonstrated that Salmonella Enteritidis strains from poultry differ in their ability to invade human intestinal cells and cause disease in orally challenged mice. Here we hypothesized that the differential virulence of Salmonella Enteritidis strains is due to the differential fitness in the adverse environments that may be encountered during infection in the host. The responses of a panel of six Salmonella Enteritidis strains to acid stress, oxidative stress, survival in egg albumen, and the ability to cause infection in chickens were analyzed. This analysis allowed classification of strains into two categories, stress-sensitive and stress-resistant, with the former showing significantly ( p < 0.05) reduced survival in acidic (gastric phase of infection) and oxidative (intestinal and systemic phase of infection) stress. Stress-sensitive strains also showed impaired intestinal colonization and systemic dissemination in orally inoculated chickens and failed to survive/grow in egg albumen. Comparative genomic hybridization microarray analysis revealed no differences at the discriminatory level of the whole gene content between stress-sensitive and stress-resistant strains. However, sequencing of rpoS, a stress-regulatory gene, revealed that one of the three stress-sensitive strains carried an insertion mutation in the rpoS resulting in truncation of r S . Finding that one of the stress-sensitive strains carried an easily identifiable small polymorphism within a stress-response gene suggests that the other strains may also have small polymorphisms elsewhere in the genome, which likely impact regulation of stress or virulence associated genes in some manner.

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Survival characteristics of Salmonella enterica serovar Enteritidis in chicken egg albumen

Cited by 59 publications

References 36 publications

RNA Sequencing Reveals Differences between the Global Transcriptomes of Salmonella enterica Serovar Enteritidis Strains with High and Low Pathogenicities

RNA Sequencing Reveals Differences between the Global Transcriptomes of Salmonella enterica Serovar Enteritidis Strains with High and Low Pathogenicities

Differential Phenotypic Diversity among Epidemic-Spanning Salmonella enterica Serovar Enteritidis Isolates from Humans or Animals

SalmonellaEnteritidis Strains from Poultry Exhibit Differential Responses to Acid Stress, Oxidative Stress, and Survival in the Egg Albumen

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