Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system

Shah, Devendra H.; Zhou, Xiaohui; Addwebi, Tarek; Davis, Margaret A.; Orfe, Lisa H.; Call, Douglas R.; Guard, Jean; Besser, Thomas E.

doi:10.1099/mic.0.044461-0

Cited by 76 publications

(97 citation statements)

References 188 publications

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“…However, when newly hatched chickens were challenged with each of the 5 serovars, all but S. Senftenberg exhibited high rates of organ invasion (Ͼ85%, versus 14% for S. Senftenberg), which were different than the in vitro intracellular survival outcomes (245). These findings were consistent with studies on S. Enteritidis strains classified as displaying either low-or high-invasive phenotypes in Caco-2 human colon tissue in vitro assays (246,247). Those studies demonstrated that when mice were orally challenged, low-invasive strains were as virulent as high-invasive strains, even though not all S. Enteritidis isolates recovered from poultry are equally pathogenic.…”

Section: The Salmonella-chicken Host Interactionsupporting

confidence: 81%

Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars

Foley

Johnson

Ricke

et al. 2013

Microbiol Mol Biol Rev

244

207

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SUMMARY Enteric pathogens such as Salmonella enterica cause significant morbidity and mortality. S. enterica serovars are a diverse group of pathogens that have evolved to survive in a wide range of environments and across multiple hosts. S. enterica serovars such as S . Typhi, S . Dublin, and S . Gallinarum have a restricted host range, in which they are typically associated with one or a few host species, while S . Enteritidis and S . Typhimurium have broad host ranges. This review examines how S. enterica has evolved through adaptation to different host environments, especially as related to the chicken host, and continues to be an important human pathogen. Several factors impact host range, and these include the acquisition of genes via horizontal gene transfer with plasmids, transposons, and phages, which can potentially expand host range, and the loss of genes or their function, which would reduce the range of hosts that the organism can infect. S . Gallinarum, with a limited host range, has a large number of pseudogenes in its genome compared to broader-host-range serovars. S. enterica serovars such as S . Kentucky and S . Heidelberg also often have plasmids that may help them colonize poultry more efficiently. The ability to colonize different hosts also involves interactions with the host's immune system and commensal organisms that are present. Thus, the factors that impact the ability of Salmonella to colonize a particular host species, such as chickens, are complex and multifactorial, involving the host, the pathogen, and extrinsic pressures. It is the interplay of these factors which leads to the differences in host ranges that we observe today.

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Section: The Salmonella-chicken Host Interactionsupporting

confidence: 81%

Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars

Foley

Johnson

Ricke

et al. 2013

Microbiol Mol Biol Rev

244

207

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“…Thus, proper assembly of flagella in S. Kentucky is required for attachment and invasion, not just the production of flagellin. These results are consistent with findings of previous studies on several poultry-associated isolates of S. enterica with mutations in flgK, flgL, and fljB genes, which exhibited invasion reduction in Caco-2 cell line compared to the parental strain (25).…”

Section: Figsupporting

confidence: 82%

Salmonella enterica Serovar Kentucky Flagella Are Required for Broiler Skin Adhesion and Caco-2 Cell Invasion

Salehi

Howe

Lawrence

et al. 2017

Appl Environ Microbiol

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Nontyphoidal Salmonella strains are the main source of pathogenic bacterial contamination in the poultry industry. Recently, Salmonella enterica serovar Kentucky has been recognized as the most prominent serovar on carcasses in poultry-processing plants. Previous studies showed that flagella are one of the main factors that contribute to bacterial attachment to broiler skin. However, the precise role of flagella and the mechanism of attachment are unknown. There are two different flagellar subunits (fliC and fljB) expressed alternatively in Salmonella enterica serovars using phase variation. Here, by making deletions in genes encoding flagellar structural subunits (flgK, fliC, and fljB), and flagellar motor (motA), we were able to differentiate the role of flagella and their rotary motion in the colonization of broiler skin and cellular attachment. Utilizing a broiler skin assay, we demonstrated that the presence of FliC is necessary for attachment to broiler skin. Expression of the alternative flagellar subunit FljB enables Salmonella motility, but this subunit is unable to mediate tight attachment. Deletion of the flgK gene prevents proper flagellar assembly, making Salmonella significantly less adherent to broiler skin than the wild type. S. Kentucky with deletions in all three structural genes, fliC, fljB, and flgK, as well as a flagellar motor mutant (motA), exhibited less adhesion and invasion of Caco-2 cells, while an fljB mutant was as adherent and invasive as the wild-type strain.IMPORTANCE In this work, we answered clearly the role of flagella in S. Kentucky attachment to the chicken skin and Caco-2 cells. We demonstrated that the presence of FliC is necessary for attachment to broiler skin. Expression of the alternative flagellar subunit FljB enables Salmonella motility, but this subunit is unable to mediate strong attachment. Deletion of the flgK gene prevents proper flagellar assembly, making Salmonella significantly less adherent to broiler skin than the wild type. S. Kentucky with deletions in all three structural genes, fliC, fljB, and flgK, as well as a flagellar motor mutant (motA), exhibited less adhesion and invasion of Caco-2 cells, while an fljB mutant was as adherent and invasive as the wild-type strain. We expect these results will contribute to the understanding of the mechanisms of Salmonella attachment to food products.

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“…Grossman et al (13) reported an association between decreased motility and decreased severity of illness in clinical isolates of S. Typhi from Indonesia. More recently, it was reported that impaired motility in four poultry-associated isolates of S. Enteritidis was associated with low invasiveness in differentiated Caco-2 cells and reduced virulence in the mouse typhoid model (33). In the present work, we screened a comprehensive collection of isolates derived from human clinical, animal, and environmental sources and found that 72 out of 266 (27%) showed total absence of motility.…”

Section: Discussionmentioning

confidence: 99%

Naturally Occurring Motility-Defective Mutants of Salmonella enterica Serovar Enteritidis Isolated Preferentially from Nonhuman Rather than Human Sources

Yim

Betancor

Martinez

et al. 2011

Appl Environ Microbiol

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Salmonellosis represents a worldwide health problem because it is one of the major causes of food-borne disease. Although motility is postulated as an important Salmonella virulence attribute, there is little information about variation in motility in natural isolates. Here we report the identification of a point mutation (T551 3 G) in motA, a gene essential for flagellar rotation, in several Salmonella enterica serovar Enteritidis field isolates. This mutation results in bacteria that can biosynthesize structurally normal but paralyzed flagella and are impaired in their capacity to invade human intestinal epithelial cells. Introduction of a wild-type copy of motA into one of these isolates restored both motility and cell invasiveness. The motA mutant triggered higher proinflammatory transcriptional responses than an aflagellate isolate in differentiated Caco-2 cells, suggesting that the paralyzed flagella are able to signal through pattern recognition receptors. A specific PCR was designed to screen for the T551 3 G mutation in a collection of 266 S. Enteritidis field isolates from a nationwide epidemic, comprising 194 from humans and 72 from other sources. We found that 72 of the 266 (27%) isolates were nonmotile, including 24.7% (48/194) of human and 33.3% (24/72) of food isolates. Among nonmotile isolates, 15 carried the T551 3 G mutation and, significantly, 13 were recovered from food, including 7 from eggs, but only 2 were from human sources. These results suggest that the presence of paralyzed flagella may impair the ability of S. Enteritidis to cause disease in the human host but does not prevent its ability to colonize chickens and infect eggs.

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Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system

Cited by 76 publications

References 188 publications

Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars

Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars

Salmonella enterica Serovar Kentucky Flagella Are Required for Broiler Skin Adhesion and Caco-2 Cell Invasion

Naturally Occurring Motility-Defective Mutants of Salmonella enterica Serovar Enteritidis Isolated Preferentially from Nonhuman Rather than Human Sources

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