Optimal noise filtering in the chemotactic response of Escherichia coli.
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ABSTRACT:
SUBMITTER: Andrews BW
PROVIDER: S-EPMC1636674 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Adaptation of the chemotaxis sensory pathway of the bacterium Escherichia coli is integral for detecting chemicals over a wide range of background concentrations, ultimately allowing cells to swim towards sources of attractant and away from repellents. Its biochemical mechanism based on methylation and demethylation of chemoreceptors has long been known. Despite the importance of adaptation for cell memory and behavior, the dynamics of adaptation are difficult to reconcile with current models of precise adaptation. Here, we follow time courses of signaling in response to concentration step changes of attractant using in vivo fluorescence resonance energy transfer measurements. Specifically, we use a condensed representation of adaptation time courses for efficient evaluation of different adaptation models. To quantitatively explain the data, we finally develop a dynamic model for signaling and adaptation based on the attractant flow in the experiment, signaling by cooperative receptor complexes, and multiple layers of feedback regulation for adaptation. We experimentally confirm the predicted effects of changing the enzyme-expression level and bypassing the negative feedback for demethylation. Our data analysis suggests significant imprecision in adaptation for large additions. Furthermore, our model predicts highly regulated, ultrafast adaptation in response to removal of attractant, which may be useful for fast reorientation of the cell and noise reduction in adaptation.
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Project description:In their natural environment, cells need to extract useful information from complex temporal signals that vary over a wide range of intensities and time scales. Here, we study how such signals are processed by Escherichia coli during chemotaxis by developing a general theoretical model based on receptor adaptation and receptor-receptor cooperativity. Measured responses to various monotonic, oscillatory, and impulsive stimuli are all explained consistently by the underlying adaptation kinetics within this model. For exponential ramp signals, an analytical solution is discovered that reveals a remarkable connection between the dependence of kinase activity on the exponential ramp rate and the receptor methylation rate function. For exponentiated sine-wave signals, spectral analysis shows that the chemotaxis pathway acts as a lowpass filter for the derivative of the signal with the cutoff frequency determined by an intrinsic adaptation time scale. For large step stimuli, we find that the recovery time is determined by the constant maximum methylation rate, which provides a natural explanation for the observed recovery time additivity. Our model provides a quantitative system-level description of the chemotaxis signaling pathway and can be used to predict E. coli chemotaxis responses to arbitrary temporal signals. This model of the receptor system reveals the molecular origin of Weber's law in bacterial chemotaxis. We further identify additional constraints required to account for the related observation that the output of this pathway is constant under exponential ramp stimuli, a feature that we call "logarithmic tracking."
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Project description: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 step-down 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 single-cell level. Our findings provide clues to an improved understanding of chemotactic adaptation.
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Project description:At high cell density, swimming bacteria exhibit collective motility patterns, self-organized through physical interactions of a however still debated nature. Although high-density behaviours are frequent in natural situations, it remained unknown how collective motion affects chemotaxis, the main physiological function of motility, which enables bacteria to follow environmental gradients in their habitats. Here, we systematically investigate this question in the model organism Escherichia coli, varying cell density, cell length, and suspension confinement. The characteristics of the collective motion indicate that hydrodynamic interactions between swimmers made the primary contribution to its emergence. We observe that the chemotactic drift is moderately enhanced at intermediate cell densities, peaks, and is then strongly suppressed at higher densities. Numerical simulations reveal that this suppression occurs because the collective motion disturbs the choreography necessary for chemotactic sensing. We suggest that this physical hindrance imposes a fundamental constraint on high-density behaviours of motile bacteria, including swarming and the formation of multicellular aggregates and biofilms.
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Project description:Chemotaxis allows bacteria to follow gradients of nutrients, environmental stimuli, and signaling molecules, optimizing bacterial growth and survival. Escherichia coli has long served as a model of bacterial chemotaxis, and the signal processing by the core of its chemotaxis pathway is well understood. However, most of the research so far has focused on one branch of chemotactic signaling, in which ligands bind to periplasmic sensory domains of transmembrane chemoreceptors and induce a conformational change that is transduced across the membrane to regulate activity of the receptor-associated kinase CheA. Here we quantitatively characterize another, receptor-independent branch of chemotactic signaling that is linked to the sugar uptake through a large family of phosphotransferase systems (PTSs). Using in vivo characterization of intracellular signaling and protein interactions, we demonstrate that signals from cytoplasmic PTS components are transmitted directly to the sensory complexes formed by chemoreceptors, CheA and an adapter protein CheW. We further conclude that despite different modes of sensing, the PTS- and receptor-mediated signals have similar regulatory effects on the conformation of the sensory complexes. As a consequence, both types of signals become integrated and undergo common downstream processing including methylation-dependent adaptation. We propose that such mode of signaling is essential for efficient chemotaxis to PTS substrates and may be common to most bacteria.
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Project description:BackgroundEscherichia coli is a widespread gut commensal and often a versatile pathogen of public health concern. E. coli are also frequently found in different environments and/or alternative secondary hosts, such as plant tissues. The lifestyle of E. coli in plants is poorly understood and has potential implications for food safety.Methods/principal findingsThis work shows that a human commensal strain of E. coli K12 readily colonizes lettuce seedlings and produces large microcolony-like cell aggregates in leaves, especially in young leaves, in proximity to the vascular tissue. Our observations strongly suggest that those cell aggregates arise from multiplication of single bacterial cells that reach those spots. We showed that E. coli isolated from colonized leaves progressively colonize lettuce seedlings to higher titers, suggesting a fast adaptation process. E. coli cells isolated from leaves presented a dramatic rise in tolerance to oxidative stress and became more chemotactic responsive towards lettuce leaf extracts. Mutant strains impaired in their chemotactic response were less efficient lettuce colonizers than the chemotactic isogenic strain. However, acclimation to oxidative stress and/or minimal medium alone failed to prime E. coli cells for enhanced lettuce colonization efficiency.Conclusion/significanceThese findings help to understand the physiological adaptation during the alternative lifestyle of E. coli in/on plant tissues.
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Project description:Studies on chemotaxis of Escherichia coli have shown that modulation of tumble frequency causes a net drift up the gradient of attractants. Recently, it has been demonstrated that the bacteria is also capable of varying its runs speed in uniform concentration of attractant. In this study, we investigate the role of swimming speed on the chemotactic migration of bacteria. To this end, cells are exposed to gradients of a non-metabolizable analogue of glucose which are sensed via the Trg sensor. When exposed to a gradient, the cells modulate their tumble duration, which is accompanied with variation in swimming speed leading to drift velocities that are much higher than those achieved through the modulation of the tumble duration alone. We use an existing intra-cellular model developed for the Tar receptor and incorporate the variation of the swimming speed along with modulation of tumble frequency to predict drift velocities close to the measured values. The main implication of our study is that E. coli not only modulates the tumble frequency, but may also vary the swimming speed to affect chemotaxis and thereby efficiently sample its nutritionally rich environment.
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Project description:BackgroundThe chemotaxis pathway in the bacterium Escherichia coli allows cells to detect changes in external ligand concentration (e.g. nutrients). The pathway regulates the flagellated rotary motors and hence the cells' swimming behaviour, steering them towards more favourable environments. While the molecular components are well characterised, the motor behaviour measured by tethered cell experiments has been difficult to interpret.ResultsWe study the effects of sensing and signalling noise on the motor behaviour. Specifically, we consider fluctuations stemming from ligand concentration, receptor switching between their signalling states, adaptation, modification of proteins by phosphorylation, and motor switching between its two rotational states. We develop a model which includes all signalling steps in the pathway, and discuss a simplified version, which captures the essential features of the full model. We find that the noise characteristics of the motor contain signatures from all these processes, albeit with varying magnitudes.ConclusionsOur analysis allows us to address how cell-to-cell variation affects motor behaviour and the question of optimal pathway design. A similar comprehensive analysis can be applied to other two-component signalling pathways.
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Project description:BackgroundCells sense chemical spatial gradients and respond by polarizing internal components. This process can be disrupted by gradient noise caused by fluctuations in chemical concentration.ResultsWe investigated how external gradient noise affects spatial sensing and response focusing on noise-filtering and the resultant tradeoffs. First, using a coarse-grained mathematical model of gradient-sensing and cell polarity, we characterized three negative consequences of noise: Inhibition of the extent of polarization, degradation of directional accuracy, and production of a noisy output polarization. Next, we explored filtering strategies and discovered that a combination of positive feedback, multiple signaling stages, and time-averaging produced good results. There was an important tradeoff, however, because filtering resulted in slower polarization. Simulations demonstrated that a two-stage filter-amplifier resulted in a balanced outcome. Then, we analyzed the effect of noise on a mechanistic model of yeast cell polarization in response to gradients of mating pheromone. This analysis showed that yeast cells likely also combine the above three filtering mechanisms into a filter-amplifier structure to achieve impressive spatial-noise tolerance, but with the consequence of a slow response time. Further investigation of the amplifier architecture revealed two positive feedback loops, a fast inner and a slow outer, both of which contributed to noise-tolerant polarization. This model also made specific predictions about how orientation performance depended upon the ratio between the gradient slope (signal) and the noise variance. To test these predictions, we performed microfluidics experiments measuring the ability of yeast cells to orient to shallow gradients of mating pheromone. The results of these experiments agreed well with the modeling predictions, demonstrating that yeast cells can sense gradients shallower than 0.1% ?m-1, approximately a single receptor-ligand molecule difference between front and back, on par with motile eukaryotic cells.ConclusionsSpatial noise impedes the extent, accuracy, and smoothness of cell polarization. A combined filtering strategy implemented by a filter-amplifier architecture with slow dynamics was effective. Modeling and experimental data suggest that yeast cells employ these elaborate mechanisms to filter gradient noise resulting in a slow but relatively accurate polarization response.
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Project description:Chemotactic eukaryotic cells are able to detect chemoattractant gradients that are both shallow and have a low background concentration. Under these conditions, the noise in the number of bound receptors can be significant and needs to be taken into account in determining the directional sensing process. Here, we quantify numerically the number of bound receptors on the membrane of a disk-shaped cell by using a numerical Monte Carlo tool. The obtained time traces of the receptor occupancy can be used as inputs for any directional sensing model. We investigate the response of the local excitation global inhibition model and a recently developed balanced inactivation model. We determine a measure for the motility of the cell for each model, based on the relevant output variable, as a function of experimental parameters, resulting in several experimentally testable predictions. Furthermore, we show that these two models behave in a qualitatively different fashion when the background concentration is varied. Thus, to properly characterize the sensitivity of cells to receptor occupancy, it is not sufficient to examine the input signal. Rather, one needs to take into account the response of the second messenger pathway.
| S-EPMC2614751 | biostudies-literature