Localization of signaling receptors maximizes cellular information acquisition in spatially structured natural environments

Cells in natural environments, such as tissue or soil, sense and respond to extracellular ligands with intri-cately structured and non-monotonic spatial distributions, sculpted by processes such as fluid flow and sub-strate adhesion. In this work, we show that spatial sensing and navigation can be optimized by adapting the spatial organization of signaling pathways to the spatial structure of the environment. We develop an infor-mation-theoretic framework for computing the optimal spatial organization of a sensing system for a given signaling environment. We find that receptor localization previously observed in cells maximizes information acquisition in simulated natural contexts, including tissue and soil. Specifically, information acquisition is maximized when receptors form localized patches at regions of maximal ligand concentration. Receptor localization extends naturally to produce a dynamic protocol for continuously redistributing signaling recep-tors, which when implemented using simple feedback, boosts cell navigation efficiency by 30-fold.

Automated summary

The ability of cells to sense and respond to extracellular ligands in natural environments can be optimized by adapting to the spatial structure of the environment. Receptor localization in cells maximizes information acquisition, and dynamic redistribution of signaling receptors enhances cell navigation efficiency.