Thermal Robustness of Signaling in Bacterial Chemotaxis

Abstract

Summary Temperature is a global factor that affects the performance of all intracellular networks. Robustness against temperature variations is thus expected to be an essential network property, particularly in organisms without inherent temperature control. Here we combine experimental analyses with computer modeling to investigate thermal robustness of signaling in chemotaxis of Escherichia coli, a relatively simple and well-established model for systems biology. We show that steady-state and kinetic pathway parameters that are essential for chemotactic performance are indeed temperature-compensated in the entire physiological range. Thermal robustness of steady-state pathway output is ensured at several levels by mutual compensation of temperature effects on activities of individual pathway components. Moreover, the effect of temperature on adaptation kinetics is counterbalanced by pre-programmed temperature dependence of enzyme synthesis and stability to achieve nearly optimal performance at the growth temperature. Similar compensatory mechanisms are expected to ensure thermal robustness in other systems.

Universal Response-Adaptation Relation in Bacterial Chemotaxis

“…This requirement arises because the time window of temporal comparisons needs to match the typical time (a few seconds) of a straight run of a bacterial cell along the gradient. The importance of a well-defined adaptation rate for the chemotaxis strategy is emphasized by existence of specific mechanisms which ensures the robustness of this rate against variations in the levels of ambient attractant (35,36), temperature (33) and gene expression (37,38). This theoretical conclusion contrasts, however, with biochemical studies demonstrating that the rate of methylation depends on the type of the receptor and on the glutamyl residue (23,39), as well as on the level of CheR (33,37,40,41).…”

“…Experimentally, the adaptation rate can be derived from measurements of the time that is needed for recovery of the pathway activity upon step-like stimulation (33,(42)(43)(44). 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).…”

“…The importance of a well-defined adaptation rate for the chemotaxis strategy is emphasized by existence of specific mechanisms which ensures the robustness of this rate against variations in the levels of ambient attractant (35,36), temperature (33) and gene expression (37,38). This theoretical conclusion contrasts, however, with biochemical studies demonstrating that the rate of methylation depends on the type of the receptor and on the glutamyl residue (23,39), as well as on the level of CheR (33,37,40,41). This discrepancy raises questions as to whether the adaptation rates for different ligands are indeed equal (or similar), as predicted by theory, and, if so, how such a universal adaptation rate is ensured despite the receptor-and residue-specific differences in the methylation rates and variations in the levels of individual receptors.…”

“…Several theoretical studies suggested that optimal chemotaxis in a gradient requires a specific adaptation rate that is defined by the gradient steepness and cell swimming velocity (31)(32)(33)(34), irrespective of the chemical nature of the ligand or of its receptor specificity. This requirement arises because the time window of temporal comparisons needs to match the typical time (a few seconds) of a straight run of a bacterial cell along the gradient.…”

Bacterial chemotaxis: information processing, thermodynamics, and behavior

“…When adaptation is precise the temporal profile of the response is largely independent of the strength of the stimulus (fold-change detection) [23,24], and in the sensitive regime receptors perform logarithmic sensing (Weber-Fechner law) [25]. Finally, the chemotaxis pathway is not only used to sense chemicals but also changes in temperature and pH [26,27].…”