Localisation and protein-protein interactions of the Helicobacter pylori taxis sensor TlpD and their connection to metabolic functions

Behrens, Wiebke; Schweinitzer, Tobias; McMurry, Jonathan L.; Loewen, P.C.; Buettner, Falk F. R.; Menz, Sarah; Josenhans, Christine

doi:10.1038/srep23582

Cited by 23 publications

(40 citation statements)

References 92 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…All antibodies detected a discrete locus at one or both cell poles in the wild-type strain, as reported previously (Fig. 6A) (30,31,34). Mutants lacking the chemoreceptors lost polar localization of the other complex members, consistent with the idea that these proteins are critical to build the chemotaxis arrays (Fig.…”

Section: Chev1 and Chewsupporting

confidence: 72%

“…Our first step was to analyze CheW and CheV1's roles in promoting the formation of the chemoreceptor-CheA complex. Both transmembrane and cytoplasmic chemoreceptors are associated with the membrane and retain CheA, which is normally cytoplasmic, at the membrane via coupling protein interactions (28)(29)(30)(31). We therefore measured the amount of CheA associated with the membrane as an indicator of overall complex formation.…”

Section: Chev1 and Chew Independently Promote Chea-chemoreceptormentioning

confidence: 99%

See 1 more Smart Citation

Cooperation of two distinct coupling proteins creates chemosensory network connections

Abedrabbo

Castellon

Collins

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Although it is appreciated that bacterial chemotaxis systems rely on coupling, also called scaffold, proteins to both connect input receptors with output kinases and build interkinase connections that allow signal amplification, it is not yet clear why many systems use more than one coupling protein. We examined the distinct functions for multiple coupling proteins in the bacterial chemotaxis system of Helicobacter pylori, which requires two nonredundant coupling proteins for chemotaxis: CheW and CheV1, a hybrid of a CheW and a phosphorylatable receiver domain. We report that CheV1 and CheW have largely redundant abilities to interact with chemoreceptors and the CheA kinase, and both similarly activated CheA’s kinase activity. We discovered, however, that they are not redundant for formation of the higher order chemoreceptor arrays that are known to form via CheA–CheW interactions. In support of this possibility, we found that CheW and CheV1 interact with each other and with CheA independent of the chemoreceptors. Therefore, it seems that some microbes have modified array formation to require CheW and CheV1. Our data suggest that multiple coupling proteins may be used to provide flexibility in the chemoreceptor array formation.

show abstract

Section: Chev1 and Chewsupporting

confidence: 72%

Section: Chev1 and Chew Independently Promote Chea-chemoreceptormentioning

confidence: 99%

Cooperation of two distinct coupling proteins creates chemosensory network connections

Abedrabbo

Castellon

Collins

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…The TlpA receptor was reported to mediate attraction to arginine and bicarbonate [16]. The TlpD chemoreceptor was reported to mediate repulsion from conditions that induce low-energy in the bacterium [17] or conditions that promote oxidative stress [18, 19]. These conditions may be triggered by low pH.…”

Section: Resultsmentioning

confidence: 99%

Multiple Acid Sensors Control Helicobacter pylori Colonization of the Stomach

et al. 2017

View full text Add to dashboard Cite

Helicobacter pylori’s ability to respond to environmental cues in the stomach is integral to its survival. By directly visualizing H. pylori swimming behavior when encountering a microscopic gradient consisting of the repellent acid and attractant urea, we found that H. pylori is able to simultaneously detect both signals, and its response depends on the magnitudes of the individual signals. By testing for the bacteria’s response to a pure acid gradient, we discovered that the chemoreceptors TlpA and TlpD are each independent acid sensors. They enable H. pylori to respond to and escape from increases in hydrogen ion concentration near 100 nanomolar. TlpD also mediates attraction to basic pH, a response dampened by another chemoreceptor TlpB. H. pylori mutants lacking both TlpA and TlpD (ΔtlpAD) are unable to sense acid and are defective in establishing colonization in the murine stomach. However, blocking acid production in the stomach with omeprazole rescues ΔtlpAD’s colonization defect. We used 3D confocal microscopy to determine how acid blockade affects the distribution of H. pylori in the stomach. We found that stomach acid controls not only the overall bacterial density, but also the microscopic distribution of bacteria that colonize the epithelium deep in the gastric glands. In omeprazole treated animals, bacterial abundance is increased in the antral glands, and gland colonization range is extended to the corpus. Our findings indicate that H. pylori has evolved at least two independent receptors capable of detecting acid gradients, allowing not only survival in the stomach, but also controlling the interaction of the bacteria with the epithelium.

show abstract

“…TlpD mediates repellent responses to oxidative stress (64). Polar localization was also lost in mutants in genes encoding chemotaxis histidine kinase CheAY2, the central metabolic enzyme aconitase AcnB and the detoxifying enzyme catalase KatA, all identified as putative interaction partners of TlpD in CoIP experiments (63). Like FrdB, AcnB contains an iron-sulfur cluster, and both proteins contribute to the tricarboxylic acid cycle.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, polar localization of TlpD, a CZB domain protein in Helicobacter pylori, has been reported in media of high energy, whereas in low-energy conditions, such as oxidative stress, localization changed toward the cell body (63). TlpD mediates repellent responses to oxidative stress (64).…”

Section: Discussionmentioning

confidence: 99%

Evidence for Escherichia coli Diguanylate Cyclase DgcZ Interlinking Surface Sensing and Adhesion via Multiple Regulatory Routes

et al. 2016

View full text Add to dashboard Cite

DgcZ is the main cyclic dimeric GMP (c-di-GMP)-producing diguanylate cyclase (DGC) controlling biosynthesis of the exopolysaccharide poly-␤-1,6-N-acetylglucosamine (poly-GlcNAc or PGA), which is essential for surface attachment of Escherichia coli. Although the complex regulation of DgcZ has previously been investigated, its primary role and the physiological conditions under which the protein is active are not fully understood. Transcription of dgcZ is regulated by the two-component system CpxAR activated by the lipoprotein NlpE in response to surface sensing. Here, we show that the negative effect of a cpxR mutation and the positive effect of nlpE overexpression on biofilm formation both depend on DgcZ. Coimmunoprecipitation data suggest several potential interaction partners of DgcZ. Interaction with FrdB, a subunit of the fumarate reductase complex (FRD) involved in anaerobic respiration and in control of flagellum assembly, was further supported by a bacterial-two-hybrid assay. Furthermore, the FRD complex was required for the increase in DgcZ-mediated biofilm formation upon induction of oxidative stress by addition of paraquat. A DgcZ-mVENUS fusion protein was found to localize at one bacterial cell pole in response to alkaline pH and carbon starvation. Based on our data and previous knowledge, an integrative role of DgcZ in regulation of surface attachment is proposed. We speculate that both DgcZ-stimulated PGA biosynthesis and interaction of DgcZ with the FRD complex contribute to impeding bacterial escape from the surface. IMPORTANCEBacterial cells can grow by clonal expansion to surface-associated biofilms that are ubiquitous in the environment but also constitute a pervasive problem related to bacterial infections. Cyclic dimeric GMP (c-di-GMP) is a widespread bacterial second messenger involved in regulation of motility and biofilm formation, and plays a primary role in bacterial surface attachment. E. coli possesses a plethora of c-di-GMP-producing diguanylate cyclases, including DgcZ. Our study expands the knowledge on the role of DgcZ in regulation of surface attachment and suggests that it interconnects surface sensing and adhesion via multiple routes. The Gram-negative bacterium Escherichia coli is a common inhabitant of the human intestine, where it usually prevents colonization by pathogenic bacteria. Nevertheless, certain pathogenic E. coli strains cause severe diarrheal and extraintestinal diseases (1). In the industrialized world, most chronic bacterial infections are caused by pathogens growing in biofilms (2). These are communities of bacterial cells embedded in an extracellular matrix, mainly composed of exopolysaccharides and flagella, and in some cases of extracellular DNA (3-5).Biofilm formation is a gradual process starting with surface sensing and attachment (6). In E. coli K-12, recognition of the surface is mediated by the outer membrane lipoprotein NlpE that activates the two-component system CpxAR (7-9). Activation of this complex results in phosphorylation of the transc...

show abstract

Localisation and protein-protein interactions of the Helicobacter pylori taxis sensor TlpD and their connection to metabolic functions

Cited by 23 publications

References 92 publications

Cooperation of two distinct coupling proteins creates chemosensory network connections

Cooperation of two distinct coupling proteins creates chemosensory network connections

Multiple Acid Sensors Control Helicobacter pylori Colonization of the Stomach

Evidence for Escherichia coli Diguanylate Cyclase DgcZ Interlinking Surface Sensing and Adhesion via Multiple Regulatory Routes

Contact Info

Product

Resources

About