Sensory transduction in
            <i>Escherichia coli</i>
            : Role of a protein methylation reaction in sensory adaptation

In Halobaeterium halobium tactic responses towards light and chemoeffectors are accompanied by changes in the methylation level of methyl-accepting chemotaxis proteins (MCP). Taxis towards green light absorbed by the bacteriorhodopsin proton pump appears to be governed by A/t H +-sensing. The addition of CCCP, an uncoupler, prevented the increase of MCP methylation in response to green light illumination, but had no effect on CH3-incorporation followed by the addition of the attractants glucose, leucine and histidine: Similarly, CCCP did not change MCP demethylation in response to blue light illumination, a repelling stimuli. The sensitivity to an uncoupler of methylation linked to AFt H+-mediated green light taxis is to be expected, while the independence of demethylation caused by the blue light of CCCP is an indication that in the latter case a specific photoreceptor governs phototaxis. Informed processing from the blue light receptor to MCP does not involve a change in the membrane potential. Halobacterium halobium photobehavior a~H+-sensing Protein methylation Blue-light taxis

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“…Attractants cause MCP methylation that represents adaptation to them, while adaptation to repellents is followed by MCP demethylation [4].…”

Section: Introductionmentioning

confidence: 99%

The role of methylation in the taxis of Halobacterium halobium to light and chemo‐effectors

1982

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“…Adaptation site residues lie on solventexposed helix faces and share a consensus nine-residue motif at which CheR and CheB must bind for catalysis (13)(14)(15). Differences in higher-order structures of the methylation helix bundle presumably govern state-specific access to the substrate sites.Those structural differences probably involve changes in substrate helix stability and changes in the packing interactions between helices of the methylation bundle (9,(16)(17)(18)(19).The critical sensory adaptation roles of the CheR and CheB enzymes have been known for decades (20)(21)(22)(23)(24)(25). Here, we report that CheR has a second function that opposes the signaling consequences of its catalytic activity.…”

mentioning

confidence: 99%

“…The critical sensory adaptation roles of the CheR and CheB enzymes have been known for decades (20)(21)(22)(23)(24)(25). Here, we report that CheR has a second function that opposes the signaling consequences of its catalytic activity.…”

mentioning

confidence: 99%

Paradoxical enhancement of chemoreceptor detection sensitivity by a sensory adaptation enzyme

Lai¹,

Han²,

Dahlquist³

et al. 2017

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

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A sensory adaptation system that tunes chemoreceptor sensitivity enables motile Escherichia coli cells to track chemical gradients with high sensitivity over a wide dynamic range. Sensory adaptation involves feedback control of covalent receptor modifications by two enzymes: CheR, a methyltransferase, and CheB, a methylesterase. This study describes a CheR function that opposes the signaling consequences of its catalytic activity. In the presence of CheR, a variety of mutant serine chemoreceptors displayed up to 40-fold enhanced detection sensitivity to chemoeffector stimuli. This response enhancement effect did not require the known catalytic activity of CheR, but did involve a binding interaction between CheR and receptor molecules. Response enhancement was maximal at low CheR:receptor stoichiometry and quantitative analyses argued against a reversible binding interaction that simply shifts the ON-OFF equilibrium of receptor signaling complexes. Rather, a short-lived CheR binding interaction appears to promote a long-lasting change in receptor molecules, either a covalent modification or conformation that enhances their response to attractant ligands.bacterial chemotaxis | receptor methyltransferase | dynamic-bundle model | signaling conformation | nonequilibrium mechanism M otile bacteria, despite their small size and simple cellular architecture, track chemical gradients in their living environments with extraordinary precision (see refs. 1 and 2 for reviews). They do so with only a handful of different proteins organized in a sensory signaling network that has stimulus integration, amplification, and memory capabilities. The extensively studied chemotaxis machinery of Escherichia coli has provided the molecular paradigm for transmembrane and intracellular signaling mechanisms in microbial chemosensory systems. This report describes a long-unrecognized activity of a central component of the E. coli chemotaxis machinery, suggesting that there are important new molecular lessons to learn from this structurally simple, yet functionally sophisticated, signaling system. E. coli senses attractant and repellent chemicals with transmembrane chemoreceptors known as methyl-accepting chemotaxis proteins (MCPs) (3). MCPs form networked arrays of signaling complexes, typically at the cell poles, that produce highly sensitive and cooperative responses to small chemoeffector concentration changes. The four MCPs of E. coli (Tsr, Tar, Tap, and Trg) have a common functional architecture comprising a periplasmic sensing domain and a cytoplasmic signaling domain (Fig. 1). An interposed HAMP domain communicates conformational changes between the sensing and signaling domains through an extended four-helix coiled-coil that contains sites for sensory adaptation adjustments of receptor signal output (4). The chemoreceptors modulate the activity of a histidine autokinase (CheA), which is stably coupled to receptors by a scaffolding protein (CheW). CheA donates its phosphoryl groups to CheY, a response regulator that in its phosphory...

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“…Memory is provided by the receptor methylation system, consisting of the methyltransferase CheR and the methylesterase CheB, which respectively methylate or demethylate receptors on four or five specific glutamate residues. CheR preferentially recognizes the inactive state of receptors and increases receptor activity through methylation, whereas CheB preferentially demethylates active receptors and thereby lowers their activity (20)(21)(22)(23)(24)(25)(26)). An additional negative feedback is provided by the CheA-mediated phosphorylation of CheB, which increases its methylesterase activity (27,28).…”

mentioning

confidence: 99%

“…Because more methyl groups are required to offset a stronger stimulus, the adaptation time depends both on the adaptation rate and on the strength of the initial stimulation (21,42). In this study, we investigated the rates of adaptation to attractants sensed by different types of receptors.…”

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confidence: 99%

Universal Response-Adaptation Relation in Bacterial Chemotaxis

2015

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The bacterial strategy of chemotaxis relies on temporal comparisons of chemical concentrations, where the probability of maintaining the current direction of swimming is modulated by changes in stimulation experienced during the recent past. A shortterm memory required for such comparisons is provided by the adaptation system, which operates through the activity-dependent methylation of chemotaxis receptors. Previous theoretical studies have suggested that efficient navigation in gradients requires a well-defined adaptation rate, because the memory time scale needs to match the duration of straight runs made by bacteria. Here we demonstrate that the chemotaxis pathway of Escherichia coli does indeed exhibit a universal relation between the response magnitude and adaptation time which does not depend on the type of chemical ligand. Our results suggest that this alignment of adaptation rates for different ligands is achieved through cooperative interactions among chemoreceptors rather than through fine-tuning of methylation rates for individual receptors. This observation illustrates a yet-unrecognized function of receptor clustering in bacterial chemotaxis. In bacterial chemotaxis, effector stimuli are detected by a set of transmembrane receptors of different specificities (1-4). Escherichia coli has five types of chemoreceptors, with Tar and Tsr being major receptors and Trg, Tap, and Aer being minor chemoreceptors. Together with the histidine kinase CheA and an adaptor protein, CheW, receptors are organized in large sensory complexes that perform most of signal processing in chemotaxis (5-9). Activities of teams of 10 to 20 individual receptors are allosterically coupled within these complexes, enabling amplification and integration of changes in the relative ligand occupancy of receptors (10-17). The integrated signaling output of the receptor complexes is subsequently converted into the stimulation-dependent phosphorylation of the response regulator CheY, which controls cell swimming behavior.The bacterial strategy of chemotaxis relies on temporal comparisons of chemoeffector concentrations. This requires a short-term memory that enables bacteria to detect changes in concentrations along the swimming track and to modify their behavior accordingly, to either continue swimming in this direction or to tumble and reorient (18,19). Memory is provided by the receptor methylation system, consisting of the methyltransferase CheR and the methylesterase CheB, which respectively methylate or demethylate receptors on four or five specific glutamate residues. CheR preferentially recognizes the inactive state of receptors and increases receptor activity through methylation, whereas CheB preferentially demethylates active receptors and thereby lowers their activity (20-26). An additional negative feedback is provided by the CheA-mediated phosphorylation of CheB, which increases its methylesterase activity (27,28). In the absence of a gradient, these feedbacks allow the system to adapt to ambient stimulation, ensuring that t...

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Sensory transduction in Escherichia coli : Role of a protein methylation reaction in sensory adaptation

Cited by 194 publications

References 19 publications

The role of methylation in the taxis of Halobacterium halobium to light and chemo‐effectors

The role of methylation in the taxis of Halobacterium halobium to light and chemo‐effectors

Paradoxical enhancement of chemoreceptor detection sensitivity by a sensory adaptation enzyme

Universal Response-Adaptation Relation in Bacterial Chemotaxis

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