Chemotaxis to the Quorum-Sensing Signal AI-2 Requires the Tsr Chemoreceptor and the Periplasmic LsrB AI-2-Binding Protein

Hegde, Manjunath; Englert, Derek L.; Schrock, Shanna; Cohn, William B.; Vogt, Christian P.; Wood, Thomas K.; Manson, Michael D.; Jayaraman, Arul

doi:10.1128/jb.01196-10

Cited by 124 publications

(119 citation statements)

References 29 publications

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“…Maltose sensitivity for chemotaxis using mutants lacking MalF (22) was 10-fold greater (0.1 vs. 1 mM) than that of strains carrying wild-type MalF (10), although still significantly higher than the K d of MBP for maltose (1-3 μM) (23). Similarly, deletion of the LrsC transporter of AI-2 increased the sensitivity of LrsB (AI-2 binding protein)-mediated chemotaxis by approximately two log orders (24). Other recent work has also found interactions between ABC transport systems and histidine sensor kinases (25,26).…”

Section: Discussionmentioning

confidence: 88%

Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals

Zhao

DeGrado³

et al. 2012

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

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Agrobacterium tumefaciens is a broad host range plant pathogen that combinatorially recognizes diverse host molecules including phenolics, low pH, and aldose monosaccharides to activate its pathogenic pathways. Chromosomal virulence gene E (chvE) encodes a periplasmic-binding protein that binds several neutral sugars and sugar acids, and subsequently interacts with the VirA/ VirG regulatory system to stimulate virulence (vir) gene expression. Here, a combination of genetics, X-ray crystallography, and isothermal calorimetry reveals how ChvE binds the different monosaccharides and also shows that binding of sugar acids is pH dependent. Moreover, the potency of a sugar for vir gene expression is modulated by a transport system that also relies on ChvE. These two circuits tune the overall system to respond to sugar concentrations encountered in vivo. Finally, using chvE mutants with restricted sugar specificities, we show that there is host variation in regard to the types of sugars that are limiting for vir induction.protein crystallization | sugar binding protein | sugar binding specificity | host recognition | ABC transporter B road host range bacterial pathogens confront a variety of problems in the context of regulating their virulence mechanisms. Because these mechanisms are usually energy intensive, the controlling system is expected to exhibit very tight regulationactivating virulence pathways under conditions that are not suitable for pathogenic activity would be wasteful (1). However, the pathogen needs to recognize diverse hosts, suggesting that the control system must be very flexible in terms of signal perception. Agrobacterium tumefaciens is a broad host range plant pathogen that has the intriguing capacity to recognize several chemically distinct types of host molecules and to activate virulence (vir) gene expression only when the appropriate combination of signals is perceived. Moreover, within each class of signals, there is unusual chemical diversity, providing an important means of broadening host range. The focus of this paper is on the periplasmic sugar binding protein encoded by the chromosomal virulence gene E (chvE) of A. tumefaciens, which recognizes diverse aldose monosaccharides including arabinose, glucose, galactose, fucose, and xylose as well as sugar acids such as galacturonic and glucuronic acids (2-4).ChvE works together with the VirA/VirG two-component system of A. tumefaciens to integrate information from several different host-derived signals and activate virulence gene expression. ChvE binds aldose monosaccharides, whereas VirA recognizes plant phenolic derivatives; low pH impinges on the system at multiple levels. Previously, we found that there was little correlation between the in vitro dissociation constants for binding of various sugars to ChvE and the corresponding efficacy of these sugars to activate vir gene expression (2). Here, we resolve this apparent paradox by considering ChvE's activity in the context of the complex interplay between pathogen and host. Specifically...

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Section: Discussionmentioning

confidence: 88%

Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals

Zhao

DeGrado³

et al. 2012

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

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“…On the basis of these studies, one hypothesis is that E. coli might use AI-2 to join groups of bacteria that produce AI-2 (Defoirdt, 2010). It is also possible that chemotaxis to AI-2 might serve to attract free-living bacteria to biofilms (Hegde et al, 2011). AI-2 is better understood in Vibrios than in other bacteria.…”

Section: Discussionmentioning

confidence: 99%

Diversity and functional analysis of luxS genes in Vibrios from marine sponges Mycale laxissima and Ircinia strobilina

2011

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Sponges harbor highly diverse and dense microbial communities, providing an environment in which bacterial signaling may be important. Quorum sensing (QS) is a cell density-dependent signaling process that bacteria employ to coordinate and regulate their gene expression. Previous studies have found that bacteria isolated from sponges are able to produce acyl-homoserine lactones (AHLs), an important class of QS molecules found in proteobacteria. Autoinducer-2 (AI-2) is a second class of QS molecule, and is considered to be an interspecies signal. However, AI-2 signaling has not been reported in sponge bacterial symbionts. In this study, degenerate primers were designed based on known Vibrio luxS sequences to amplify the luxS genes encoding AI-2 synthases of several Vibrio isolates from marine sponges Mycale laxissima and Ircinia strobilina. All the vibrios isolated from these two sponges had luxS genes and were able to produce signals with AI-2 activity as detected using a biological reporter. A novel group of luxS sequences was found, thus extending the known diversity of luxS genes. One isolate was chosen for further analysis of its luxS gene by expression of the gene in Escherichia coli DH5a and by characterization of the profile of AI-2 activity. This work provides the first information about luxS genes and AI-2 activity in sponge-associated bacterial communities.

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“…Both bacteria and archaea employ chemoreceptors known as methyl-accepting chemotaxis proteins (MCPs) to monitor their chemical environments (3,61). E. coli has four canonical MCPs: Tsr mediates attractant responses to serine and to the interspecies quorum signal, AI-2 (19,47); Tar mediates attractant responses to aspartate and to maltose (17,47); Tap mediates attractant responses to dipeptides and to pyrimidines (28,31); and Trg mediates attractant responses to ribose and galactose (16). These transmembrane receptors function as homodimers of ϳ550-residue subunits, each comprising a periplasmic sensing domain, flanked by two membrane-spanning helices (TM1 and TM2), and a cytoplasmic kinase control domain (Fig.…”

mentioning

confidence: 99%

Phenol Sensing by Escherichia coli Chemoreceptors: a Nonclassical Mechanism

Parkinson

2011

Journal of Bacteriology

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The four transmembrane chemoreceptors of Escherichia coli sense phenol as either an attractant (Tar) or a repellent (Tap, Trg, and Tsr). In this study, we investigated the Tar determinants that mediate its attractant response to phenol and the Tsr determinants that mediate its repellent response to phenol. Tar molecules with lesions in the aspartate-binding pocket of the periplasmic domain, with a foreign periplasmic domain (from Tsr or from several Pseudomonas chemoreceptors), or lacking nearly the entire periplasmic domain still mediated attractant responses to phenol. Similarly, Tar molecules with the cytoplasmic methylation and kinase control domains of Tsr still sensed phenol as an attractant. Additional hybrid receptors with signaling elements from both Tar and Tsr indicated that the transmembrane (TM) helices and HAMP domain determined the sign of the phenol-sensing response. Several amino acid replacements in the HAMP domain of Tsr, particularly attractant-mimic signaling lesions at residue E248, converted Tsr to an attractant sensor of phenol. These findings suggest that phenol may elicit chemotactic responses by diffusing into the cytoplasmic membrane and perturbing the structural stability or position of the TM bundle helices, in conjunction with structural input from the HAMP domain. We conclude that behavioral responses to phenol, and perhaps to temperature, cytoplasmic pH, and glycerol, as well, occur through a general sensing mechanism in chemoreceptors that detects changes in the structural stability or dynamic behavior of a receptor signaling element. The structurally sensitive target for phenol is probably the TM bundle, but other behaviors could target other receptor elements.Chemotaxis, the movement of an organism toward or away from chemicals, is an important adaptive behavior of motile prokaryotes, such as Escherichia coli. Both bacteria and archaea employ chemoreceptors known as methyl-accepting chemotaxis proteins (MCPs) to monitor their chemical environments (3, 61). E. coli has four canonical MCPs: Tsr mediates attractant responses to serine and to the interspecies quorum signal, 47); Tar mediates attractant responses to aspartate and to maltose (17, 47); Tap mediates attractant responses to dipeptides and to pyrimidines (28, 31); and Trg mediates attractant responses to ribose and galactose (16). These transmembrane receptors function as homodimers of ϳ550-residue subunits, each comprising a periplasmic sensing domain, flanked by two membrane-spanning helices (TM1 and TM2), and a cytoplasmic kinase control domain (Fig. 1). The cytoplasmic region of MCPs consists of a signal-converting HAMP domain at the membrane interface and a long coiledcoil four-helix bundle (Fig. 1). The highly conserved membrane-distal tip of the cytoplasmic bundle contains residues that promote interactions with other MCP molecules, with the signaling kinase CheA, and with CheW, which couples CheA autophosphorylation activity to receptor control (4,23,50). CheA, in turn, regulates the phosphorylation state of Che...

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Chemotaxis to the Quorum-Sensing Signal AI-2 Requires the Tsr Chemoreceptor and the Periplasmic LsrB AI-2-Binding Protein

Cited by 124 publications

References 29 publications

Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals

Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals

Diversity and functional analysis of luxS genes in Vibrios from marine sponges Mycale laxissima and Ircinia strobilina

Phenol Sensing by Escherichia coli Chemoreceptors: a Nonclassical Mechanism

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