Genome Sequence of the Thermotolerant Foodborne Pathogen Salmonella enterica Serovar Senftenberg ATCC 43845 and Phylogenetic Analysis of Loci Encoding Increased Protein Quality Control Mechanisms

Nguyen, Scott V.; Harhay, Gregory P.; Bono, James L.; Smith, Timothy P. L.; Harhay, Dayna M.

doi:10.1128/msystems.00190-16

Cited by 26 publications

(36 citation statements)

References 47 publications

(86 reference statements)

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“…This suggests that the heat tolerance is often a phenotypic phenomenon and that the isolates that we studied simply had a higher subpopulation of heat-tolerant survivors. In contrast, Nguyen et al recently identified a heat resistance island in Salmonella Senftenberg, indicating a genotypic basis for heat tolerance in some salmonellae (54). We did not find this island in our heat-tolerant isolates, which is unsurprising, as to date it has been identified only in Salmonella Senftenberg (54).…”

Section: Discussioncontrasting

confidence: 91%

“…In contrast, Nguyen et al recently identified a heat resistance island in Salmonella Senftenberg, indicating a genotypic basis for heat tolerance in some salmonellae (54). We did not find this island in our heat-tolerant isolates, which is unsurprising, as to date it has been identified only in Salmonella Senftenberg (54). We also did not investigate promoter sequences for mutations which might have led to enhanced gene expression, but we recognize that this could contribute to differential expression.…”

Section: Discussioncontrasting

confidence: 80%

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Salmonella enterica subsp. enterica Serovar Heidelberg Food Isolates Associated with a Salmonellosis Outbreak Have Enhanced Stress Tolerance Capabilities

Etter

West

Burnett

et al. 2019

Appl Environ Microbiol

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Salmonella enterica serovar Heidelberg is currently the 12th most common serovar of Salmonella enterica causing salmonellosis in the United States and results in twice the average incidence of blood infections caused by nontyphoidal salmonellae. Multiple outbreaks of salmonellosis caused by Salmonella Heidelberg resulted from the same poultry processor, which infected 634 people during 2013 and 2014. The hospitalization and invasive illness rates were 38% and 15%, respectively. We hypothesized that the outbreak strains of Salmonella Heidelberg had enhanced stress tolerance and virulence capabilities. We sourced nine food isolates collected during the outbreak investigation and three reference isolates to assess their tolerance to heat and sanitizers, ability to attach to abiotic surfaces, and invasiveness in vitro. We performed RNA sequencing on three isolates (two outbreak-associated isolates and a reference Salmonella Heidelberg strain) with various levels of heat tolerance to gain insight into the mechanism behind the isolates' enhanced heat tolerance. We also performed genomic analyses to determine the genetic relationships among the outbreak isolates. Ultimately, we determined that (i) six Salmonella Heidelberg isolates associated with the foodborne outbreak had enhanced heat tolerance, (ii) one outbreak isolate with enhanced heat tolerance also had an enhanced biofilm-forming ability under stressful conditions, (iii) exposure to heat stress increased the expression of Salmonella Heidelberg multidrug efflux and virulence genes, and (iv) outbreak-associated isolates were likely transcriptionally primed to better survive processing stresses and, potentially, to cause illness. IMPORTANCE This study provides a deep analysis of the intrinsic stress tolerance and virulence capabilities of Salmonella Heidelberg that may have contributed to the length and severity of a recent salmonellosis outbreak. Additionally, this study provides a comprehensive analysis of the transcriptomic response of S. enterica strains to heat stress conditions and compares baseline stationary-phase gene expression among outbreak-and non-outbreak-associated Salmonella Heidelberg isolates. These data can be used in assay development to screen isolates for stress tolerance and subsequent survival. This study adds to our understanding of the strains associated with the outbreak and informs ongoing regulatory discussions on Salmonella in poultry.

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Section: Discussioncontrasting

confidence: 91%

Section: Discussioncontrasting

confidence: 80%

Salmonella enterica subsp. enterica Serovar Heidelberg Food Isolates Associated with a Salmonellosis Outbreak Have Enhanced Stress Tolerance Capabilities

Etter

West

Burnett

et al. 2019

Appl Environ Microbiol

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“…ClpG/ ClpG GI might have developed in bacteria indwelling a demanding ecological niche in parallel to the Hsp70-ClpB system, or ClpG/ ClpG GI is an evolutionary younger protein. Recent acquisition of ClpG GI homologs, often on plasmids and in more than one copy, by unconventional pathogens associated with industrial and clinical settings (see also below) suggests that certain man-made environments provide a strong selection pressure aiding predominantly the spread of the dna-shsp20 GI -clpG GI core unit (59,60).…”

Section: Discussionmentioning

confidence: 99%

Stand-alone ClpG disaggregase confers superior heat tolerance to bacteria

Lee

Franke

Kamal

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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AAA+ disaggregases solubilize aggregated proteins and confer heat tolerance to cells. Their disaggregation activities crucially depend on partner proteins, which target the AAA+ disaggregases to protein aggregates while concurrently stimulating their ATPase activities. Here, we report on two potent ClpG disaggregase homologs acquired through horizontal gene transfer by the species and subsequently abundant clone C. ClpG exhibits high, stand-alone disaggregation potential without involving any partner cooperation. Specific molecular features, including high basal ATPase activity, a unique aggregate binding domain, and almost exclusive expression in stationary phase distinguish ClpG from other AAA+ disaggregases. Consequently, ClpG largely contributes to heat tolerance of primarily in stationary phase and boosts heat resistance 100-fold when expressed in This qualifies ClpG as a potential persistence and virulence factor in .

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“…Boll et al (16) compared the functions of the 15-kb LHR1 and the 19-kb LHR2. Deletion and transconjugation experiments in E. coli and Salmonella demonstrated that the effect of the 15-kb LHR1 on heat resistance is equal to or greater than the effect of the 19-kb LHR2 proteins (16,17,21); proteins that are necessary for heat resistance must thus be encoded by both variants of the LHR. In LHR2, orf3 to orf5, which are truncated in LHR1, are replaced by functional cardiolipin synthase and FtsH protease genes.…”

Section: Discussionmentioning

confidence: 99%

Functional Analysis of Genes Comprising the Locus of Heat Resistance in Escherichia coli

Mercer

Nguyen

et al. 2017

Appl Environ Microbiol

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The locus of heat resistance (LHR) is a 15- to 19-kb genomic island conferring exceptional heat resistance to organisms in the family , including pathogenic strains of and The complement of LHR-comprising genes that is necessary for heat resistance and the stress-induced or growth-phase-induced expression of LHR-comprising genes are unknown. This study determined the contribution of the seven LHR-comprising genes, ,, ,, , and by comparing the heat resistances of strains harboring plasmid-encoded derivatives of the different LHRs in these genes. (Genes carry a subscript "GI" [genomic island] if an ortholog of the same gene is present in genomes of) LHR-encoded heat shock proteins sHSP20, ClpK, and sHSP are not sufficient for the heat resistance phenotype; YfdX1, YfdX2, and HdeD are necessary to complement the LHR heat shock proteins and to impart a high level of resistance. Deletion of ,, and from plasmid-encoded copies of the LHR did not significantly affect heat resistance. The effect of the growth phase and the NaCl concentration on expression from the putative LHR promoter p2 was determined by quantitative reverse transcription-PCR and by a plasmid-encoded p2:GFP promoter fusion. The expression levels of exponential- and stationary-phase cells were not significantly different, but the addition of 1% NaCl significantly increased LHR expression. Remarkably, LHR expression in was dependent on a chromosomal copy of In conclusion, this study improved our understanding of the genes required for exceptional heat resistance in and factors that increase their expression in food. The locus of heat resistance (LHR) is a genomic island conferring exceptional heat resistance to several foodborne pathogens. The exceptional level of heat resistance provided by the LHR questions the control of pathogens by current food processing and preparation techniques. The function of LHR-comprising genes and their regulation, however, remain largely unknown. This study defines a core complement of LHR-encoded proteins that are necessary for heat resistance and demonstrates that regulation of the LHR in requires a chromosomal copy of the gene encoding EvgA. This study provides insight into the function of a transmissible genomic island that allows otherwise heat-sensitive enteric bacteria, including pathogens, to lead a thermoduric lifestyle and thus contributes to the detection and control of heat-resistant enteric bacteria in food.

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Genome Sequence of the Thermotolerant Foodborne Pathogen Salmonella enterica Serovar Senftenberg ATCC 43845 and Phylogenetic Analysis of Loci Encoding Increased Protein Quality Control Mechanisms

Cited by 26 publications

References 47 publications

Salmonella enterica subsp. enterica Serovar Heidelberg Food Isolates Associated with a Salmonellosis Outbreak Have Enhanced Stress Tolerance Capabilities

Salmonella enterica subsp. enterica Serovar Heidelberg Food Isolates Associated with a Salmonellosis Outbreak Have Enhanced Stress Tolerance Capabilities

Stand-alone ClpG disaggregase confers superior heat tolerance to bacteria

Functional Analysis of Genes Comprising the Locus of Heat Resistance in Escherichia coli

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