Bacteria use spatial sensing to direct chemotaxis on surfaces

Planktonic bacteria navigate chemical gradients using temporal sensing to detect changes in concentration over time as they swim. Here we show that surface-attached bacteria use a fundamentally different mode of sensing during chemotaxis. We combined microfluidic experiments, massively parallel cell tracking, and fluorescent reporters to study how Pseudomonas aeruginosa senses chemical gradients during pili-based "twitching" chemotaxis on surfaces. First, we asked whether surface-attached cells use temporal sensing by exposing them to temporal chemical gradients generated via Taylor-Aris dispersion. However, we find that temporal changes in concentration do not induce changes in motility, indicating that twitching cells do not sense chemical gradients like swimming bacteria do. We, therefore, designed experiments to test whether cells can detect chemical gradients across the length of their bodies. In these experiments, we follow the localisation of a fluorescent protein fusion to quantify the chemotactic behaviour of stationary cells in an alternating chemical gradient. We find that P. aeruginosa cells can directly sense differences in concentration across the lengths of their bodies, even in the presence of strong temporal fluctuations. Our work reveals that P. aeruginosa cells are capable of spatial sensing, thus overturning the widely held notion that bacterial cells are too small to directly sense chemical gradients in space.