Response rescaling in bacterial chemotaxis

Sensory systems rescale their response sensitivity upon adaptation according to simple strategies that recur in processes as diverse as single-cell signaling, neural network responses, and whole-organism perception. Here, we study response rescaling in Escherichia coli chemotaxis, where adaptation dynamically tunes the cells’ motile response during searches for nutrients. Using in vivo fluorescence resonance energy transfer (FRET) measurements on immobilized cells, we demonstrate that the design of this prokaryotic signaling network follows the fold-change detection (FCD) strategy, responding faithfully to the shape of the input profile irrespective of its absolute intensity. Using a microfluidics-based assay for free swimming cells, we confirm intensity-independent gradient responses at the behavioral level. By theoretical analysis, we identify a set of sufficient conditions for FCD in E. coli chemotaxis, which leads to the prediction that the adaptation timescale is invariant with respect to the background input level. Additional FRET experiments confirm that the adaptation timescale is invariant over an ∼10,000-fold range of background concentrations. These observations in a highly optimized bacterial system support the concept that FCD represents a robust sensing strategy for spatial searches. To our knowledge, these experiments provide a unique demonstration of FCD in any biological sensory system.

[1]  H. Berg,et al.  Functional interactions between receptors in bacterial chemotaxis , 2004, Nature.

[2]  Massimo Vergassola,et al.  Bacterial strategies for chemotaxis response , 2010, Proceedings of the National Academy of Sciences.

[3]  Fred Rieke,et al.  Review the Challenges Natural Images Pose for Visual Adaptation , 2022 .

[4]  Dennis Bray,et al.  The Chemotactic Behavior of Computer-Based Surrogate Bacteria , 2007, Current Biology.

[5]  H. Berg,et al.  Temporal comparisons in bacterial chemotaxis. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Uri Alon,et al.  Dynamics and variability of ERK2 response to EGF in individual living cells. , 2009, Molecular cell.

[7]  Roman Stocker,et al.  Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches , 2008, Proceedings of the National Academy of Sciences.

[8]  H. Berg,et al.  A modular gradient-sensing network for chemotaxis in Escherichia coli revealed by responses to time-varying stimuli , 2010, Molecular systems biology.

[9]  J. Adler,et al.  The Range of Attractant Concentrations for Bacterial Chemotaxis and the Threshold and Size of Response over This Range , 1973, The Journal of general physiology.

[10]  Roman Stocker,et al.  Bacterial chemotaxis in linear and nonlinear steady microfluidic gradients. , 2010, Nano letters.

[11]  S S Stevens,et al.  Neural events and psychophysical law. , 1971, Science.

[12]  H. Mao,et al.  A sensitive, versatile microfluidic assay for bacterial chemotaxis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[13]  S. Laughlin A Simple Coding Procedure Enhances a Neuron's Information Capacity , 1981, Zeitschrift fur Naturforschung. Section C, Biosciences.

[14]  Nikita Vladimirov,et al.  Chemotaxis: how bacteria use memory , 2009, Biological chemistry.

[15]  Gustav Theodor Fechner,et al.  Elements of psychophysics , 1966 .

[16]  G. Wadhams,et al.  Making sense of it all: bacterial chemotaxis , 2004, Nature Reviews Molecular Cell Biology.

[17]  J. Doyle,et al.  Robust perfect adaptation in bacterial chemotaxis through integral feedback control. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Victor Sourjik,et al.  In vivo measurement by FRET of pathway activity in bacterial chemotaxis. , 2007, Methods in enzymology.

[19]  Ned S Wingreen,et al.  Variable sizes of Escherichia coli chemoreceptor signaling teams , 2008, Molecular systems biology.

[20]  J. Changeux,et al.  ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL. , 1965, Journal of molecular biology.

[21]  Lea Goentoro,et al.  Evidence that fold-change, and not absolute level, of beta-catenin dictates Wnt signaling. , 2009, Molecular cell.

[22]  H. Berg,et al.  Receptor sensitivity in bacterial chemotaxis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Mingming Wu,et al.  A hydrogel-based microfluidic device for the studies of directed cell migration. , 2007, Lab on a chip.

[24]  Yuhai Tu,et al.  Modeling the chemotactic response of Escherichia coli to time-varying stimuli , 2008, Proceedings of the National Academy of Sciences.

[25]  H. Berg,et al.  A miniature flow cell designed for rapid exchange of media under high-power microscope objectives. , 1984, Journal of general microbiology.

[26]  J. S. Parkinson,et al.  Bacterial chemoreceptors: high-performance signaling in networked arrays. , 2008, Trends in biochemical sciences.

[27]  Eduardo Sontag,et al.  Fold-change detection and scalar symmetry of sensory input fields , 2010, Proceedings of the National Academy of Sciences.

[28]  P. Gennes Chemotaxis: the role of internal delays , 2004, European Biophysics Journal.

[29]  H. Berg,et al.  Impulse responses in bacterial chemotaxis , 1982, Cell.

[30]  Damon A. Clark,et al.  The bacterial chemotactic response reflects a compromise between transient and steady-state behavior. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[31]  H. Berg,et al.  Osmotic stress mechanically perturbs chemoreceptors in Escherichia coli. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  U. Alon,et al.  The incoherent feedforward loop can provide fold-change detection in gene regulation. , 2009, Molecular cell.

[33]  Y. Tu,et al.  Logarithmic sensing in Escherichia coli bacterial chemotaxis. , 2009, Biophysical journal.