Perfect and near-perfect adaptation in a model of bacterial chemotaxis.

The signaling apparatus mediating bacterial chemotaxis can adapt to a wide range of persistent external stimuli. In many cases, the bacterial activity returns to its prestimulus level exactly, and this perfect adaptability is robust against variations in various chemotaxis protein concentrations. We model the bacterial chemotaxis signaling pathway, from ligand binding to CheY phosphorylation. By solving the steady-state equations of the model analytically, we derive a full set of conditions for the system to achieve perfect adaptation. The conditions related to the phosphorylation part of the pathway are discovered for the first time, while other conditions are generalizations of the ones found in previous works. Sensitivity of the perfect adaptation is evaluated by perturbing these conditions. We find that, even in the absence of some of the perfect adaptation conditions, adaptation can be achieved with near-perfect precision as a result of the separation of scales in both chemotaxis protein concentrations and reaction rates, or specific properties of the receptor distribution in different methylation states. Since near-perfect adaptation can be found in much larger regions of the parameter space than that defined by the perfect adaptation conditions, their existence is essential to understand robustness in bacterial chemotaxis.

[1]  D. Bray,et al.  Computer simulation of the phosphorylation cascade controlling bacterial chemotaxis. , 1993, Molecular biology of the cell.

[2]  Karen A. Fahrner,et al.  Control of direction of flagellar rotation in bacterial chemotaxis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  S. Asakura,et al.  Two-state model for bacterial chemoreceptor proteins. The role of multiple methylation. , 1984, Journal of molecular biology.

[4]  H. Othmer,et al.  Oscillatory cAMP signaling in the development of Dic-tyostelium discoideum , 1998 .

[5]  M. Simon,et al.  Attenuation of sensory receptor signaling by covalent modification. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[6]  D. Bray,et al.  Receptor clustering as a cellular mechanism to control sensitivity , 1998, Nature.

[7]  G L Hazelbauer,et al.  Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[8]  J. Falke,et al.  Evidence That Both Ligand Binding and Covalent Adaptation Drive a Two-State Equilibrium in the Aspartate Receptor Signaling Complex , 2001, The Journal of general physiology.

[9]  Ann M Stock,et al.  Molecular Information Processing: Lessons from Bacterial Chemotaxis* , 2002, The Journal of Biological Chemistry.

[10]  C. J.,et al.  Predicting Temporal Fluctuations in an Intracellular Signalling Pathway , 1998 .

[11]  Uri Alon,et al.  Response regulator output in bacterial chemotaxis , 1998, The EMBO journal.

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

[13]  S. Khan,et al.  Response tuning in bacterial chemotaxis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. Koshland,et al.  Tuning the responsiveness of a sensory receptor via covalent modification. , 1991, The Journal of biological chemistry.

[15]  S. Leibler,et al.  Robustness in simple biochemical networks , 1997, Nature.

[16]  D. Koshland,et al.  Mutagenic studies of the interaction between the aspartate receptor and methyltransferase from Escherichia coli. , 1994, The Journal of biological chemistry.

[17]  D. Bray,et al.  A free-energy-based stochastic simulation of the Tar receptor complex. , 1999, Journal of molecular biology.

[18]  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.

[19]  A. Bren,et al.  How Signals Are Heard during Bacterial Chemotaxis: Protein-Protein Interactions in Sensory Signal Propagation , 2000, Journal of bacteriology.

[20]  S. Leibler,et al.  An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. , 2000, Science.

[21]  H. Berg,et al.  Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking , 1972, Nature.

[22]  D. Koshland,et al.  Interactions between the Methylation Sites of the Escherichia coli Aspartate Receptor Mediated by the Methyltransferase (*) , 1995, The Journal of Biological Chemistry.

[23]  J. Stock,et al.  Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. , 1991, The Journal of biological chemistry.

[24]  S. Chervitz,et al.  The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. , 1997, Annual review of cell and developmental biology.

[25]  J. S. Parkinson,et al.  A model of excitation and adaptation in bacterial chemotaxis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[26]  M. Surette,et al.  Receptor‐mediated protein kinase activation and the mechanism of transmembrane signaling in bacterial chemotaxis , 1997, The EMBO journal.

[27]  U. Alon,et al.  Robustness in bacterial chemotaxis , 2022 .

[28]  Ann M Stock,et al.  Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Uri Alon,et al.  Robust amplification in adaptive signal transduction networks , 2001 .