An Unorthodox Sensory Adaptation Site in the Escherichia coli Serine Chemoreceptor

Han, Xuesheng; Parkinson, John S.

doi:10.1128/jb.01164-13

Cited by 26 publications

(37 citation statements)

References 38 publications

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“…1). In Tsr dimers E sites bias receptor output toward a kinase-OFF state, whereas Q residues mimic methylated E sites (Em) and shift output toward a kinase-ON state (1,9). In UU2567 (R − B − ), wild-type Tsr subunits encoded by plasmid pPA114 or plasmid pRR53 retain their [QEQEE] residue pattern and produce a serine response with a K 1/2 of ∼17 μM.…”

Section: Resultsmentioning

confidence: 99%

“…The HAMP-MH interplay poises the two bundles for stimulus responses: Attractants enhance HAMP stability to initiate a kinase-OFF output response; a subsequent methylation increase restores kinase-ON output during sensory adaptation. CheR preferentially acts on receptors in the OFF state; CheB preferentially acts on receptors in the ON state (1,9). AS1 (shown) and AS1′ are the N-terminal HAMP helices; AS2 and AS2′ (shown) are the C-terminal HAMP helices.…”

Section: Resultsmentioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

“…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 homodimeric serine chemoreceptor (Tsr) contains five adaptation sites per subunit (8,9), two of which are genetically encoded as glutaminyl (Q) residues, which mimic the signaling properties of Em sites (Fig. 1).…”

mentioning

confidence: 99%

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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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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

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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Regulation of the chemotaxis histidine kinase CheA: A structural perspective

Muok¹,

Briegel²,

Crane³

2020

Biochimica et Biophysica Acta (BBA) - Biomembranes

104

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Bacteria sense and respond to their environment through a highly conserved assembly of transmembrane chemoreceptors (MCPs), the histidine kinase (CheA), and the coupling protein CheW, hereafter termed "the chemosensory array". In recent years, great strides have been made in understanding the architecture of the underlying chemosensory arrays and how these assemblies engender sensitive and cooperative responses. Nonetheless, a central outstanding question surrounds how receptors modulate the activity of the chemotaxis kinase CheA, the enzymatic output of the sensory system. With a focus on recent advances, we summarize the current understanding of array structure and function to comment on the molecular mechanism by which CheA, receptors and CheW generate the high sensitivity, gain and dynamic range emblematic of bacterial chemotaxis. The complexity of the chemosensory arrays has motivated investigation with many different approaches. In particular, structural methods, genetics, cellular activity assays, nanodisc technology and cryo-electron tomography have provided advances that bridge length scales and connect molecular mechanism to cellular function. Given the high degree of component integration in the chemosensory arrays, we ultimately aim to understand how such networked molecular interactions generate a whole that is truly greater than the sum of its parts.

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Single-Cell E. coli Response to an Instantaneously Applied Chemotactic Signal

Sagawa

Kikuchi

Inoue

et al. 2014

Biophysical Journal

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In response to an attractant or repellant, an Escherichia coli cell controls the rotational direction of its flagellar motor by a chemotaxis system. When an E. coli cell senses an attractant, a reduction in the intracellular concentration of a chemotaxis protein, phosphorylated CheY (CheY-P), induces counterclockwise (CCW) rotation of the flagellar motor, and this cellular response is thought to occur in several hundred milliseconds. Here, to measure the signaling process occurring inside a single E. coli cell, including the recognition of an attractant by a receptor cluster, the inactivation of histidine kinase CheA, and the diffusion of CheY and CheY-P molecules, we applied a serine stimulus by instantaneous photorelease from a caged compound and examined the cellular response at a temporal resolution of several hundred microseconds. We quantified the clockwise (CW) and CCW durations immediately after the photorelease of serine as the response time and the duration of the response, respectively. The results showed that the response time depended on the distance between the receptor and motor, indicating that the decreased CheY-P concentration induced by serine propagates through the cytoplasm from the receptor-kinase cluster toward the motor with a timing that is explained by the diffusion of CheY and CheY-P molecules. The response time included 240 ms for enzymatic reactions in addition to the time required for diffusion of the signaling molecule. The measured response time and duration of the response also revealed that the E. coli cell senses a similar serine concentration regardless of whether the serine concentration is increasing or decreasing. These detailed quantitative findings increase our understanding of the signal transduction process that occurs inside cells during bacterial chemotaxis.

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An Unorthodox Sensory Adaptation Site in the Escherichia coli Serine Chemoreceptor

Cited by 26 publications

References 38 publications

Paradoxical enhancement of chemoreceptor detection sensitivity by a sensory adaptation enzyme

Paradoxical enhancement of chemoreceptor detection sensitivity by a sensory adaptation enzyme

Regulation of the chemotaxis histidine kinase CheA: A structural perspective

Single-Cell E. coli Response to an Instantaneously Applied Chemotactic Signal

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