Contribution of the Salmonella enterica KdgR Regulon to Persistence of the Pathogen in Vegetable Soft Rots

George, Andrée S.; González, Isaí Salas; Lorca, Graciela L.; Teplitski, Max

doi:10.1128/aem.03355-15

Cited by 10 publications

(16 citation statements)

References 40 publications

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“…Having previously reported that kdgR alone is not responsible for the growth of S . Typhimurium 14028 in soft-rotted tomatoes ( 24 ) and in light of the fact that the starch-scavenging hypothesis was proven null, we performed a high-throughput assay in order to identify the full complement of genes responsible for this interaction. Transposon sequencing (Tn-Seq) has become an important tool for untangling complex metabolic networks in Salmonella spp.…”

Section: Resultsmentioning

confidence: 99%

“…Previously, we established that the deletion of the kdgR gene, which codes for a repressor of cell wall degradation and uptake of monomers and dimers resulting from the plant cell wall breakdown, was beneficial to the growth of S. enterica serovar Typhimurium strain ATCC 14028 ( S . Typhimurium 14028) in soft rot ( 24 ). However, further investigation of the KdgR regulon did not offer a conclusive explanation for its role in the ability of Salmonella spp.…”

Section: Introductionmentioning

confidence: 99%

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Interactions of Salmonella enterica Serovar Typhimurium and Pectobacterium carotovorum within a Tomato Soft Rot

George

Cox

Desai

et al. 2018

Appl Environ Microbiol

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Salmonella spp. are remarkably adaptable pathogens, and this adaptability allows these bacteria to thrive in a variety of environments and hosts. The mechanisms with which these pathogens establish within a niche amid the native microbiota remain poorly understood. Here, we aimed to uncover the mechanisms that enable Salmonella enterica serovar Typhimurium strain ATCC 14028 to benefit from the degradation of plant tissue by a soft rot plant pathogen, Pectobacterium carotovorum. The hypothesis that in the soft rot, the liberation of starch (not utilized by P. carotovorum) makes this polymer available to Salmonella spp., thus allowing it to colonize soft rots, was tested first and proven null. To identify the functions involved in Salmonella soft rot colonization, we carried out transposon insertion sequencing coupled with the phenotypic characterization of the mutants. The data indicate that Salmonella spp. experience a metabolic shift in response to the changes in the environment brought on by Pectobacterium spp. and likely coordinated by the csrBC small regulatory RNA. While csrBC and flhD appear to be of importance in the soft rot, the global two-component system encoded by barA sirA (which controls csrBC and flhDC under laboratory conditions) does not appear to be necessary for the observed phenotype. Motility and the synthesis of nucleotides and amino acids play critical roles in the growth of Salmonella spp. in the soft rot.IMPORTANCE Outbreaks of produce-associated illness continue to be a food safety concern. Earlier studies demonstrated that the presence of phytopathogens on produce was a significant risk factor associated with increased Salmonella carriage on fruits and vegetables. Here, we genetically characterize some of the requirements for interactions between Salmonella and phytobacteria that allow Salmonella spp. to establish a niche within an alternate host (tomato). Pathways necessary for nucleotide synthesis, amino acid synthesis, and motility are identified as contributors to the persistence of Salmonella spp. in soft rots.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Interactions of Salmonella enterica Serovar Typhimurium and Pectobacterium carotovorum within a Tomato Soft Rot

George

Cox

Desai

et al. 2018

Appl Environ Microbiol

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“…One of these mutations mapped to kdgR (9), a transcriptional regulator that modulates uptake of distinct carbon sources. Intriguingly, the KdgR regulon favors persistence of serovar Typhimurium in vegetable soft rots in association with defined phytopathogens such as Pectobacterium carotovorum (77). This role in persistence was linked to increased uptake of carbon sources derived from pectin degradation and utilization of the Entner-Doudoroff pathway, both regulated by KdgR (77).…”

Section: The Scv As a Suitable Niche To Prolong Host Infection In A Nmentioning

confidence: 99%

“…Intriguingly, the KdgR regulon favors persistence of serovar Typhimurium in vegetable soft rots in association with defined phytopathogens such as Pectobacterium carotovorum (77). This role in persistence was linked to increased uptake of carbon sources derived from pectin degradation and utilization of the Entner-Doudoroff pathway, both regulated by KdgR (77). Mammalian cells do not produce pectin, so it is tempting to speculate that the action of KdgR in intracellular serovar Typhimurium is related to the hydrolysis and product utilization of some yet unknown polysaccharide.…”

Section: The Scv As a Suitable Niche To Prolong Host Infection In A Nmentioning

confidence: 99%

Salmonella Intracellular Lifestyles and Their Impact on Host-to-Host Transmission

Pucciarelli

Portillo

2019

Microbial Transmission

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More than a century ago, infections by Salmonella were already associated with foodborne enteric diseases with high morbidity in humans and cattle. Intestinal inflammation and diarrhea are hallmarks of infections caused by nontyphoidal Salmonella serovars, and these pathologies facilitate pathogen transmission to the environment. In those early times, physicians and microbiologists also realized that typhoid and paratyphoid fever caused by some Salmonella serovars could be transmitted by "carriers," individuals outwardly healthy or at most suffering from some minor chronic complaint. In his pioneering study of the nontyphoidal serovar Typhimurium in 1967, Takeuchi published the first images of intracellular bacteria enclosed by membrane-bound vacuoles in the initial stages of the intestinal epithelium penetration. These compartments, called Salmonella-containing vacuoles, are highly dynamic phagosomes with differing biogenesis depending on the host cell type. Single-cell studies involving real-time imaging and gene expression profiling, together with new approaches based on genetic reporters sensitive to growth rate, have uncovered unprecedented heterogeneous responses in intracellular bacteria. Subpopulations of intracellular bacteria displaying fast, reduced, or no growth, as well as cytosolic and intravacuolar bacteria, have been reported in both in vitro and in vivo infection models. Recent investigations, most of them focused on the serovar Typhimurium, point to the selection of persisting bacteria inside macrophages or following an autophagy attack in fibroblasts. Here, we discuss these heterogeneous intracellular lifestyles and speculate on how these disparate behaviors may impact host-to-host transmissibility of Salmonella serovars.

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“…Although human pathogens may benefit from the release of substrates from damaged cells in plant lesions ( Aruscavage et al, 2010 ; Kyle et al, 2010 ; Goudeau et al, 2013 ; George et al, 2016 ), physicochemical conditions resulting from the injury per se and from the plant defense response to wounding or infection may also contribute to the outcome of a contamination event at the site of injury. Our transcriptomic studies previously revealed that in addition to responding to oxidative and antimicrobial stress in romaine lettuce leaf lysate and in cut leaf tissue, EcO157 mounted a response to osmotic stress by upregulation of the betA and betB genes for GB synthesis while the otsBA genes for production of the osmoprotectant trehalose were strongly downregulated ( Kyle et al, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

Escherichia coli O157:H7 Converts Plant-Derived Choline to Glycine Betaine for Osmoprotection during Pre- and Post-harvest Colonization of Injured Lettuce Leaves

et al. 2017

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Plant injury is inherent to the production and processing of fruit and vegetables. The opportunistic colonization of damaged plant tissue by human enteric pathogens may contribute to the occurrence of outbreaks of foodborne illness linked to produce. Escherichia coli O157:H7 (EcO157) responds to physicochemical stresses in cut lettuce and lettuce lysates by upregulation of several stress response pathways. We investigated the tolerance of EcO157 to osmotic stress imposed by the leakage of osmolytes from injured lettuce leaf tissue. LC-MS analysis of bacterial osmoprotectants in lettuce leaf lysates and wound washes indicated an abundant natural pool of choline, but sparse quantities of glycine betaine and proline. Glycine betaine was a more effective osmoprotectant than choline in EcO157 under osmotic stress conditions in vitro. An EcO157 mutant with a deletion of the betTIBA genes, which are required for biosynthesis of glycine betaine from imported choline, achieved population sizes twofold lower than those of the parental strain (P < 0.05) over the first hour of colonization of cut lettuce in modified atmosphere packaging (MAP). The cell concentrations of the betTIBA mutant also were 12-fold lower than those of the parental strain (P < 0.01) when grown in hypertonic lettuce lysate, indicating that lettuce leaf cellular contents provide choline for osmoprotection of EcO157. To demonstrate the utilization of available choline by EcO157 for osmoadaptation in injured leaf tissue, deuterated (D-9) choline was introduced to wound sites in MAP lettuce; LC-MS analysis revealed the conversion of D9-choline to D-9 glycine betaine in the parental strain, but no significant amounts were observed in the betTIBA mutant. The EcO157 ΔbetTIBA-ΔotsBA double mutant, which is additionally deficient in de novo synthesis of the compatible solute trehalose, was significantly less fit than the parental strain after their co-inoculation onto injured lettuce leaves and MAP cut lettuce. However, its competitive fitness followed a different time-dependent trend in MAP lettuce, likely due to differences in O2 content, which modulates betTIBA expression. Our study demonstrates that damaged lettuce leaf tissue does not merely supply EcO157 with substrates for proliferation, but also provides the pathogen with choline for its survival to osmotic stress experienced at the site of injury.

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Contribution of the Salmonella enterica KdgR Regulon to Persistence of the Pathogen in Vegetable Soft Rots

Cited by 10 publications

References 40 publications

Interactions of Salmonella enterica Serovar Typhimurium and Pectobacterium carotovorum within a Tomato Soft Rot

Interactions of Salmonella enterica Serovar Typhimurium and Pectobacterium carotovorum within a Tomato Soft Rot

Salmonella Intracellular Lifestyles and Their Impact on Host-to-Host Transmission

Escherichia coli O157:H7 Converts Plant-Derived Choline to Glycine Betaine for Osmoprotection during Pre- and Post-harvest Colonization of Injured Lettuce Leaves

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