Adapt locally and act globally: strategy to maintain high chemoreceptor sensitivity in complex environments

Lan, Ganhui; Schulmeister, Sonja; Sourjik, Victor; Tu, Yuhai

doi:10.1038/msb.2011.8

Cited by 45 publications

(86 citation statements)

References 60 publications

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“…Compared to that in the wild type, the RA relation was particularly strongly affected in the Tsr-only cells. This is consistent with previous observations of inefficient adaptation to high levels of Tsr ligands (18,44,50) and of the serine-induced cross-methylation of Tar (51).…”

Section: Universal Relation Between Chemotactic Response and Adaptatisupporting

confidence: 82%

“…Such interactions are predicted to couple not only the activities of different receptors but also their methylation kinetics (51,53), because the binding of an attractant molecule to any of the receptors in the allosteric signaling team reduces the activity of the entire team and therefore initially stimulates increased methylation of all receptors. Although due to the incomplete coupling between receptors such cross-methylation is only transient (51,56), it is apparently sufficient to align the adaptation rates for different ligands in the case of the subsaturating stimulation in our experiments. Because the stimulation experienced by cells swimming in a gradient is even weaker than the stimuli used in our experiments, the observed RA alignment is highly relevant for chemotaxis.…”

Section: Discussionmentioning

confidence: 99%

“…Instead, the alignment of the RA relation for different ligands can be easily explained by the Monod-Wyman-Changeux (MWC) model of allosteric interactions between different receptors in sensory complexes (12,14,16,51,53). Because these interactions couple the activity states of different receptors, the inactivation of one receptor by its ligand leads to the inactivation of other receptors in the same complex.…”

Section: Universal Relation Between Chemotactic Response and Adaptatimentioning

confidence: 99%

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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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Section: Universal Relation Between Chemotactic Response and Adaptatisupporting

confidence: 82%

Section: Discussionmentioning

confidence: 99%

Section: Universal Relation Between Chemotactic Response and Adaptatimentioning

confidence: 99%

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Universal Response-Adaptation Relation in Bacterial Chemotaxis

2015

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“…In particular, we quantified two features of adaptation: (i) abruptness (the degree to which return to prestimulus behavior occurs within a small number of run/tumble events) and (ii) overshoot (the degree of excessive response before the return to prestimulus behavior). Though abruptness and overshoot have been previously reported in the literature (9,16,(21)(22)(23), they have not yet been characterized in detail. Here, we quantify both features in response to both step-up and step-down stimuli across a broad range of stimulus strengths.…”

mentioning

confidence: 94%

“…In general, an overshoot response may occur whenever different components of the network adapt at different rates. A recent theoretical model of the chemotaxis network (23) postulates that the overshoot response is caused by the differences in methylation kinetics between different types of receptors. Interestingly, one of the studies mentioned above (19) was conducted using a mutant strain that only expressed a single receptor type, potentially explaining why an overshoot was not reported.…”

Section: Overshootmentioning

confidence: 99%

Chemotactic adaptation kinetics of individual Escherichia coli cells

Min

Mears

Golding

et al. 2012

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

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Escherichia coli chemotaxis serves as a paradigm for the way living cells respond and adapt to changes in their environment. The chemotactic response has been characterized at the level of individual flagellar motors and in populations of swimming cells. However, it has not been previously possible to quantify accurately the adaptive response of a single, multiflagellated cell. Here, we use our recently developed optical trapping technique to characterize the swimming behavior of individual bacteria as they respond to sudden changes in the chemical environment. We follow the adaptation kinetics of E. coli to varying magnitudes of step-up and stepdown changes in concentration of chemoattractant. We quantify two features of adaptation and how they vary with stimulus strength: abruptness (the degree to which return to prestimulus behavior occurs within a small number of run/tumble events) and overshoot (the degree of excessive response before the return to prestimulus behavior). We also characterize the asymmetry between step-up and step-down responses, observed at the singlecell level. Our findings provide clues to an improved understanding of chemotactic adaptation.bacterial chemotaxis | optical tweezers | single cell studies

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Decoding the chemotactic signal

Thomas

Kleist

Volkman

2018

Journal of Leukocyte Biology

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From an individual bacterium to the cells that compose the human immune system, cellular chemotaxis plays a fundamental role in allowing cells to navigate, interpret, and respond to their environments. While many features of cellular chemotaxis are shared among systems as diverse as bacteria and human immune cells, the machinery that guides the migration of these model organisms varies widely. In this article, we review current literature on the diversity of chemoattractant ligands, the cell surface receptors that detect and process chemotactic gradients, and the link between signal recognition and the regulation of cellular machinery that allow for efficient directed cellular movement. These facets of cellular chemotaxis are compared among E. coli, Dictyostelium discoideum, and mammalian neutrophils to derive organizational principles by which diverse cell systems sense and respond to chemotactic gradients to initiate cellular migration.

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Adapt locally and act globally: strategy to maintain high chemoreceptor sensitivity in complex environments

Abstract: In bacterial chemotaxis, several types of receptors form mixed clusters. Receptor adaptation is shown to depend on the receptor's own conformational state rather than on the cluster's global activity, enabling cells to differentiate stimuli in complex environments.

Cited by 45 publications

References 60 publications

Universal Response-Adaptation Relation in Bacterial Chemotaxis

Universal Response-Adaptation Relation in Bacterial Chemotaxis

Chemotactic adaptation kinetics of individual Escherichia coli cells

Decoding the chemotactic signal

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