A direct-sensing galactose chemoreceptor recently evolved in invasive strains of Campylobacter jejuni

Day, Christopher J.; King, Rebecca M.; Shewell, Lucy K.; Tram, Greg; Najnin, Tahria; Hartley-Tassell, Lauren E.; Wilson, Jennifer C.; Fleetwood, Aaron D.; Zhulin, Igor B.; Korolik, Victoria

doi:10.1038/ncomms13206

Cited by 54 publications

(63 citation statements)

References 51 publications

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“…In this study, we demonstrated that the periplasmic CACHE domain of CqsR QS receptor is involved in signal sensing; and we also identified a common metabolite ethanolamine as a signal that regulates the CqsR QS signaling pathway in V. cholerae . The periplasmic CACHE domain is common in many chemotaxis receptors and other membrane bound regulators (28); and CACHE domain proteins have been shown to interact with a variety of chemical compounds (28, 35, 41, 46–48). While CACHE domain has been shown to interact with quaternary ammonium including choline (an ethanolamine analog that CqsR does not interact) to control chemotaxis (49, 50), our study provided an example where a CACHE domain interacts with an amino alcohol (i.e., ethanolamine) to regulate QS gene expression.…”

Section: Discussionmentioning

confidence: 99%

Ethanolamine regulates CqsR quorum-sensing signaling inVibrio cholerae

Watve

Barrasso

et al. 2019

Preprint

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17The pathogen that causes cholera, Vibrio cholerae, uses the cell-cell communication process 18 known as quorum sensing (QS) to regulate virulence factor production and biofilm formation in 19 response to changes in population density and complexity. QS is mediated through the detection 20 of extracellular chemical signals called autoinducers. Four histidine kinases, LuxPQ, CqsS, CqsR 21 and VpsS, have been identified as receptors to activate the key QS regulator LuxO at low cell 22 density. At high cell density, detection of autoinducers by these receptors leads to deactivation of 23 LuxO, resulting in population-wide gene expression changes. While the cognate autoinducers that 24 regulate the activity of CqsS and LuxQ are known, the signals that regulate CqsR have not been 25 determined. Here we show that the common metabolite ethanolamine specifically interacts with 26 the ligand-binding CACHE domain of CqsR in vitro and induces the high cell-density QS response 27through CqsR kinase inhibition in V. cholerae cells. We also identified residues in the CqsR 28 CACHE domain important for ethanolamine detection and signal transduction. Moreover, 29 mutations disrupting endogenous ethanolamine production in V. cholerae delay the onset of, but 30 do not abolish, the high cell-density QS gene expression. Finally, we demonstrate that modulation 31 of CqsR QS response by ethanolamine occurs inside animal hosts. Our findings suggest that V. 32 cholerae uses CqsR as a dual-function receptor to integrate information from the self-made signals 33 as well as exogenous ethanolamine as an environmental cue to modulate QS response. 34 IMPORTANCE 35Many bacteria use quorum sensing to regulate cellular processes that are important for their 36 survival and adaptation to different environments. Quorum sensing usually depends on the 37 detection on chemical signals called autoinducers made endogenously by the bacteria. We show 38 here ethanolamine, a common metabolite made by various bacteria and eukaryotes, can modulate 39 the activity of one of the quorum-sensing receptors in Vibrio cholerae, the etiological agent of the 40 disease cholera. Our results raise the possibility that V. cholerae or other quorum-sensing bacteria 41 can combine environmental sensing and quorum sensing to control group behaviors.42 43 44 Quorum sensing (QS) is used by a wide variety of bacteria to coordinate population-wide 45 changes in behaviors in response to cell density (1). Vibrio cholerae, which causes the diarrheal 46 disease cholera in the human host, uses QS to regulate virulence factor production, biofilm 47 formation, Type VI secretion, metabolic regulation, and natural competence to maintain 48 competitive fitness in various environments (2-10). Four parallel QS signaling systems pathways 49 have been identified in V. cholerae that rely on a phosphorelay to regulate downstream gene 50 expression (11) (Figure 1). At low cell-density (LCD), four histidine kinases CqsS, LuxPQ, CqsR, 51 and VpsS function in parallel to phosphorylate LuxO...

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Section: Discussionmentioning

confidence: 99%

Ethanolamine regulates CqsR quorum-sensing signaling inVibrio cholerae

Watve

Barrasso

et al. 2019

Preprint

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“…In contrast to E. coli and Salmonella , C. jejuni has a more complex chemosensory repertoire and more sophisticated signaling control pathways, which make it an interesting model for signal transduction studies (Lertsethtakarn et al ., ; Day et al ., ). Compared to the 5 chemoreceptors in E. coli and 4 in its close relative Helicobacter pylori , C. jejuni species possess ~10 chemoreceptors, designated as transducer‐like proteins (Tlps) and 2 aerotaxis receptors (Aer1‐2) (Marchant et al ., ; Day et al ., ).…”

Section: Introductionmentioning

confidence: 99%

The novel regulators CheP and CheQ control the core chemotaxis operon cheVAW in Campylobacter jejuni

Cha

Chen

et al. 2018

Molecular Microbiology

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Summary Campylobacter jejuni is the leading cause of foodborne gastrointestinal illness worldwide, and chemotaxis plays an important role in its host colonization and pathogenesis. Although many studies on chemotaxis have focused on the physical organization and signaling mechanism of the system’s protein complex, much less is known about the transcriptional regulation of its components. Here, we describe two novel regulators, CJJ81176_0275 and CJJ81176_0276 (designated as CheP and CheQ), which specifically activate the transcription of the chemotaxis core genes cheV, cheA and cheW in C. jejuni and they are also essential for chemotactic responses. CheP has a single HD‐related output domain (HDOD) domain and can promote CheQ binding to the cheVAW operon promoter through a protein‐protein interaction. Mutagenesis analyses identified key residues critical for CheP function and/or interaction with CheQ. Further structural characterization of CheQ revealed a novel fold with strong positive surface charges that allow for its DNA binding. These findings reveal the gene regulatory mechanism of the chemotaxis system in an important bacterial pathogen and provide potential anti‐virulence targets for campylobacteriosis treatment. In addition, ChePQ is an example of how proteins with the widespread but functionally obscure HDOD can coordinate with a signal output DNA‐binding protein/domain to regulate the expression of important signaling pathways.

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“…A number of C. jejuni chemoreceptors have been shown to have a higher affinity for either CheV or CheW in C. jejuni . The Tlp2, Tlp3 (CcmL), Tlp4 paralogues and Tlp11 (CcrG) chemoreceptor signalling domains have been shown to interact non-preferentially with either CheV or CheW proteins [13-15], whereas the Tlp1 chemoreceptor has demonstrated strong interactions with only the CheV homologue [16].…”

Section: Introductionmentioning

confidence: 99%

Assigning a role for chemosensory signal transduction inCampylobacter jejunibiofilms using a combined omics approach

Korolik

Tram

Klare

et al. 2019

Preprint

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AbstractBiofilms serve as a protective mechanism for bacteria to cope with environmental stress. Whilst ordinarily a fastidious organism, it has been long suggested that C. jejuni is able to utilise this mode of growth as a way to transmit infection from the avian host to humans. Herein, we undertook a combinatorial approach to examine differential expression of C. jejuni genes and protein abundance during biofilm formation. RNA sequencing and proteomics via quantitative liquid chromatography – tandem mass spectrometry (LC-MS/MS) revealed biofilm growth induced a substantial rearrangement of the C. jejuni transcriptome and proteome, with ∼600 genes differentially expressed in biofilms compared to planktonic cells. Biofilm-induced genes / proteins were those involved in iron metabolism and acquisition, cell division, glycan production and attachment, while those repressed were associated with metabolism, amino acid uptake and utilisation, and large tracts of the chemotaxis pathway.We further examined the role of chemotaxis in C. jejuni biofilm formation by assessing the behaviour of isogenic strains with deletions of the cheV and cheW genes. Both ΔcheV and ΔcheW exhibited a significant decrease in directed motility when compared to wild-type C. jejuni. Both mutants also demonstrated an increase in autoagglutination ability and increased biofilm formation. A subtle difference was also observed between the phenotypes of ΔcheV and ΔcheW mutants, both in motility and biofilm formation. This suggests roles for the CheV and CheW signal transduction proteins and may present signal transduction as a potential method for modulating C. jejuni biofilm formation.Author summaryCampylobacter jejuni is a gastroenteric bacterium that is responsible for most cases of bacterial food poisoning in the developed world. The organism commonly resides in avian reservoirs and is passed to humans through contaminated poultry and animal products. Ordinarily, C. jejuni requires a strict set of conditions in order to survive and cause infections in humans. Biofilms are a method of bacterial growth that may provide shielding from harsh environments and provide an important link between reservoirs and human hosts. In this study, we have utilised a multi-platform approach to compare gene expression and protein abundance in planktonic C. jejuni cells and those growing as a biofilm. We subsequently focused on the chemosensory system of C. jejuni and demonstrated that signal transduction proteins play a role in biofilm formation. Our work has provided a broad profile of which genes are important to C. jejuni biofilms and that the chemosensory pathway has an influence on biofilm formation.

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A direct-sensing galactose chemoreceptor recently evolved in invasive strains of Campylobacter jejuni

Cited by 54 publications

References 51 publications

Ethanolamine regulates CqsR quorum-sensing signaling inVibrio cholerae

Ethanolamine regulates CqsR quorum-sensing signaling inVibrio cholerae

The novel regulators CheP and CheQ control the core chemotaxis operon cheVAW in Campylobacter jejuni

Assigning a role for chemosensory signal transduction inCampylobacter jejunibiofilms using a combined omics approach

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