Dataset Information

Flagellar Motility Is Critical for Salmonella enterica Serovar Typhimurium Biofilm Development.

ABSTRACT: The food-borne pathogen Salmonella enterica serovar Typhimurium (S. Typhimurium) causes self-limiting gastroenteritis in humans and is not easily eradicated because it often attaches to suitable surfaces to form biofilms that have high resistance to disinfectants and antimicrobials. To develop an alternative strategy for the treatment of biofilms, it is necessary to further explore the effects of flagellar motility on the development process of Salmonella biofilms. Here, we constructed flagella mutants (?flgE and ?fliC) to systematically study this process. By comparing them with wild-type strains, we found that these mutants lacking flagellar motility form fewer biofilms in the early stage, and the formed mature biofilms contain more cells and extracellular polymeric substances (EPS). In addition, fewer mutant cells adhered to glass plates compared with wild-type cells even after 6 h of incubation, suggesting that flagellar motility plays a significant role in preliminary cell-surface interactions. More importantly, the motility of wild-type strain was greatly decreased when they were treated with carbonyl cyanide m-chlorophenylhydrazone, which inhibited flagellar motility and reduced biofilm formation, as in the case of the ?flgE mutant. Overall, these findings suggest that flagellar motility plays an important role in Salmonella biofilm initiation and maturation, which can help us to counteract the mechanisms involved in biofilm formation and to develop more rational control strategies.

SUBMITTER: Wang F

PROVIDER: S-EPMC7509047 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Flagellar Motility Is Critical for Salmonella enterica Serovar Typhimurium Biofilm Development.

Wang Feiying F Deng Le L Huang Fangfang F Wang Zefeng Z Lu Qiujun Q Xu Chenran C

Frontiers in microbiology 20200909

The food-borne pathogen Salmonella enterica serovar Typhimurium (S. Typhimurium) causes self-limiting gastroenteritis in humans and is not easily eradicated because it often attaches to suitable surfaces to form biofilms that have high resistance to disinfectants and antimicrobials. To develop an alternative strategy for the treatment of biofilms, it is necessary to further explore the effects of flagellar motility on the development process of Salmonella biofilms. Here, we ...[more]

PMID: 33013719

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Project description:Production of flagella is costly and subject to global multilayered regulation, which is reflected in the hierarchical control of flagellar production in many bacterial species. For Salmonella enterica serovar Typhimurium and its relatives, global regulation of flagellar production primarily occurs through the control of flhDC transcription and mRNA translation. In this study, the roles of the homologous multidrug resistance regulators MarA, SoxS, Rob, and RamA (constituting the mar-sox-rob regulon in S Typhimurium) in regulating flagellar gene expression were explored. Each of these regulators was found to inhibit flagellar gene expression, production of flagella, and motility. To different degrees, repression via these transcription factors occurred through direct interactions with the flhDC promoter, particularly for MarA and Rob. Additionally, SoxS repressed flagellar gene expression via a posttranscriptional pathway, reducing flhDC translation. The roles of these transcription factors in reducing motility in the presence of salicylic acid were also elucidated, adding a genetic regulatory element to the response of S Typhimurium to this well-characterized chemorepellent. Integration of flagellar gene expression into the mar-sox-rob regulon in S Typhimurium contrasts with findings for closely related species such as Escherichia coli, providing an example of plasticity in the mar-sox-rob regulon throughout the Enterobacteriaceae family.IMPORTANCE The mar-sox-rob regulon is a large and highly conserved stress response network in the Enterobacteriaceae family. Although it is well characterized in E. coli, the extent of this regulon in related species is unclear. Here, the control of costly flagellar gene expression is connected to the mar-sox-rob regulon of S Typhimurium, contrasting with the E. coli regulon model. These findings demonstrate the flexibility of the mar-sox-rob regulon to accommodate novel regulatory targets, and they provide evidence for its broader regulatory role within this family of diverse bacteria.

Project description:Many bacteria are motile only when nutrients are scarce. In contrast, Salmonella enterica serovar Typhimurium is motile only when nutrients are plentiful, suggesting that this bacterium uses motility for purposes other than foraging, most likely for host colonization. In this study, we investigated how nutrients affect motility in S. enterica and found that they tune the fraction of motile cells. In particular, we observed coexisting populations of motile and nonmotile cells, with the distribution being determined by the concentration of nutrients in the growth medium. Interestingly, S. enterica responds not to a single nutrient but apparently to a complex mixture of them. Using a combination of experimentation and mathematical modeling, we investigated the mechanism governing this behavior and found that it results from two antagonizing regulatory proteins, FliZ and YdiV. We also found that a positive feedback loop involving the alternate sigma factor FliA is required, although its role appears solely to amplify FliZ expression. We further demonstrate that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. Together, these results uncover a new facet of the regulation of the flagellar genes in S. enterica and further demonstrate how bacteria employ phenotypic diversity as a general mechanism for adapting to change in their environment.Many bacteria employ flagella for motility. These bacteria are often not constitutively motile but become so only in response to specific environmental cues. The most common is nutrient starvation. Interestingly, in Salmonella enterica serovar Typhimurium, nutrients enhance the expression of flagella, suggesting that motility is used for purposes other than foraging. In this work, we investigated how nutrients affect motility in S. enterica and found that nutrients tune the fraction of motile cells within a population. Using both experimental and mathematical analysis, we determined the mechanism governing this tunable response. We further demonstrated that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. These results reveal a new facet of motility in S. enterica and demonstrate that nutrients determine not only where these bacteria swim but also the fraction of them that do so.

Project description:UnlabelledOne of the important virulence properties of the pathogen is its ability to travel to a favorable environment, cross the viscous mucus barrier (intestinal barrier for enteric pathogens), and reach the epithelia to initiate pathogenesis with the help of an appendage, like flagella. Nonetheless, flagella can act as an "Achilles heel," revealing the pathogen's presence to the host through the stimulation of innate and adaptive immune responses. We assessed whether curcumin, a dietary polyphenol, could alter the motility of Salmonella, a foodborne pathogen. It reduced the motility of Salmonella enterica serovar Typhimurium by shortening the length of the flagellar filament (from ∼8 μm to ∼5 μm) and decreasing its density (4 or 5 flagella/bacterium instead of 8 or 9 flagella/bacterium). Upon curcumin treatment, the percentage of flagellated bacteria declined from ∼84% to 59%. However, no change was detected in the expression of the flagellin gene and protein. A fluorescence binding assay demonstrated binding of curcumin to the flagellar filament. This might make the filament fragile, breaking it into smaller fragments. Computational analysis predicted the binding of curcumin, its analogues, and its degraded products to a flagellin molecule at an interface between domains D1 and D2. Site-directed mutagenesis and a fluorescence binding assay confirmed the binding of curcumin to flagellin at residues ASN120, ASP123, ASN163, SER164, ASN173, and GLN175.ImportanceThis work, to our knowledge the first report of its kind, examines how curcumin targets flagellar density and affects the pathogenesis of bacteria. We found that curcumin does not affect any of the flagellar synthesis genes. Instead, it binds to the flagellum and makes it fragile. It increases the torsional stress on the flagellar filament that then breaks, leaving fewer flagella around the bacteria. Flagella, which are crucial ligands for Toll-like receptor 5, are some of the most important appendages of Salmonella Curcumin is an important component of turmeric, which is a major spice used in Asian cooking. The loss of flagella can, in turn, change the pathogenesis of bacteria, making them more robust and fit in the host.

Dataset Information

Flagellar Motility Is Critical for Salmonella enterica Serovar Typhimurium Biofilm Development.

Publications

Flagellar Motility Is Critical for <i>Salmonella enterica</i> Serovar Typhimurium Biofilm Development.

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