Two-state model for bacterial chemoreceptor proteins: The role of multiple methylation

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Abstract

To help understand the bacterial chemotactic response of excitation and adaptation, we propose a simple two-state model for receptor proteins (methyl-accepting chemotaxis proteins), in the light of evidence that they undergo multiple methylation in a preferred order. The model includes the following assumptions. (1) The receptor protein is in rapid equilibrium between two conformations, S and T, and the equilibrium shifts towards the T form as the number of methyl groups increases. (2) Attractants bind to the S form of the receptor, repellents bind to the T form, and both classes of ligand shift the ST equilibrium according to the mass-action law. (3) The S form of the receptor accepts methyl groups one by one in a definite order, while the T form releases the methyl groups in the reverse order. Methylation and demethylation are slow reactions, and changes in the total number of methyl groups lag behind shifts in the ST equilibrium. (4) The pattern of bacterial swimming at any moment is determined by the partition of the receptor between the two conformations, with tumbling frequency being a monotonically increasing function of the total T fraction of the receptor. This model shows that, if the receptor satisfies two sets of relationships imposed on its equilibrium and kinetic constants, it can maintain the steady-state total T fraction essentially constant over a broad range of ligand concentration, enabling cells to adapt to large changes in chemical environment. A stepwise change in ligand concentration leads to a rapid change in the total T fraction (excitation), followed by a slow relaxation process (adaptation). Computer simulations have been made of the whole response process, employing a receptor with six methylation sites per molecule and assuming simple sets of parameters. The results are in general agreement with published data on receptor methylation, as well as with a variety of observations of bacterial chemoresponse. Multiple methylation of the receptor proves to be necessary for the cells to respond sensitively to environmental changes.

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