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Assigning a role for chemosensory signal transduction in Campylobacter jejuni biofilms using a combined omics approach.

ABSTRACT: Biofilms of the gastroenteric pathogen C. jejuni may serve an important role in the transmission of infection from reservoirs of infection to humans. Herein, we undertook a combinatorial approach examining differential gene expression and protein abundance during biofilm formation in C. jejuni. Biofilms induced a substantial rearrangement of the C. jejuni transcriptome and proteome, with ~600 genes differentially expressed when compared to planktonic cells. Genes and proteins induced in biofilms were involved in iron metabolism and acquisition, cell division, glycan production and attachment, while those repressed were associated with metabolism, amino acid usage, and large tracts of the chemotaxis pathway. We further examined the role of chemotaxis in C. jejuni biofilm formation by examining isogenic strains with deletions of the cheV and cheW signal transduction genes. Both ?cheV and ?cheW exhibited a significant decrease in directed motility when compared to wild-type C. jejuni as well as demonstrating an increase in autoagglutination ability and biofilm formation. A subtle difference was also observed between the phenotypes of ?cheV and ?cheW mutants, both in motility and biofilm formation. This suggests roles for CheV and CheW and may present signal transduction as a potential method for modulating C. jejuni biofilm formation.

SUBMITTER: Tram G

PROVIDER: S-EPMC7176700 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Assigning a role for chemosensory signal transduction in Campylobacter jejuni biofilms using a combined omics approach.

Tram Greg G Klare William P WP Cain Joel A JA Mourad Basem B Cordwell Stuart J SJ Day Christopher J CJ Korolik Victoria V

Scientific reports 20200422 1

Biofilms of the gastroenteric pathogen C. jejuni may serve an important role in the transmission of infection from reservoirs of infection to humans. Herein, we undertook a combinatorial approach examining differential gene expression and protein abundance during biofilm formation in C. jejuni. Biofilms induced a substantial rearrangement of the C. jejuni transcriptome and proteome, with ~600 genes differentially expressed when compared to planktonic cells. Genes and proteins induced in biofilms ...[more]

PMID: 32321947

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Project description:UnlabelledMany polarly flagellated bacteria require similar two-component regulatory systems (TCSs) and σ(54) to activate transcription of genes essential for flagellar motility. Herein, we discovered that in addition to the flagellar type III secretion system (T3SS), the Campylobacter jejuni flagellar MS ring and rotor are required to activate the FlgSR TCS. Mutants lacking the FliF MS ring and FliG C ring rotor proteins were as defective as T3SS mutants in FlgSR- and σ(54)-dependent flagellar gene expression. Also, FliF and FliG required each other for stability, which is mediated by atypical extensions to the proteins. A FliF mutant that presumably does not interact with the T3SS protein FlhA did not support flagellar gene transcription, suggesting that FliF-T3SS interactions are essential to generate a signal sensed by the cytoplasmic FlgS histidine kinase. Furthermore, the flagellar T3SS was required for FlgS to immunoprecipitate with FliF and FliG. We propose a model whereby the flagellar T3SS facilitates FliF and FliG multimerization into the MS ring and rotor. As a result, these flagellar structures form a cytoplasmic complex that interacts with and is sensed by FlgS. The synthesis of these structures appears to be a regulatory checkpoint in flagellar biogenesis that the FlgS kinase monitors to initiate signal transduction that activates σ(54) and expression of genes required for the next stage of flagellation. Given that other polar flagellates have flagellar transcriptional hierarchies that are organized similarly as in C. jejuni, this regulatory checkpoint may exist in a broad range of bacteria to influence similar TCSs and flagellar gene transcription.ImportanceDespite the presence of numerous two-component regulatory systems (TCSs) in bacteria, direct signals sensed by TCSs to activate signal transduction are known for only a minority. Polar flagellates, including Pseudomonas, Vibrio, Helicobacter, and Campylobacter species, require a similar TCS and σ(54) for flagellar gene transcription, but the activating signals for these TCSs are unknown. We explored signals that activate the Campylobacter jejuni FlgSR TCS to initiate σ(54)-dependent flagellar gene transcription. Our discoveries suggest that the FlgS histidine kinase monitors the formation of the flagellar type III secretion system and the surrounding MS and C rings. The synthesis of these structures creates a regulatory checkpoint in flagellar biogenesis that is sensed by FlgS to ensure proper transcription of the next set of genes for subsequent steps in flagellation. Given the conservation of flagellar-associated TCSs and transcriptional cascades in polar flagellates, this regulatory checkpoint in flagellar biogenesis likely impacts flagellation in a broad range of bacteria.

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Dataset Information

Assigning a role for chemosensory signal transduction in Campylobacter jejuni biofilms using a combined omics approach.

Publications

Assigning a role for chemosensory signal transduction in Campylobacter jejuni biofilms using a combined omics approach.

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