Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability

The structure of bacterial biofilms depends on environmental conditions, such as availability of nutrients, during biofilm formation. In turn, variations in biofilm structure in part reflect differences in bacterial motility during early biofilm formation. Pseudomonas aeruginosa deprived of nutrients remain dispersed on a surface, whereas cells supplemented with additional nutrients cluster and form microcolonies. At the single-cell scale, how bacteria modify their motility to favour distinct life cycle outcomes remains poorly understood. High-throughput algorithms were used to track thousands of P. aeruginosa moving using type-IV pili (TFP) on surfaces in varying nutrient conditions and hence identify four distinct motility types. A minimal stochastic model was used to reproduce the TFP-driven motility types. We report that P. aeruginosa cells differently deploy TFP to alter the distribution of motility types under different nutrient conditions. Bacteria preferentially crawl unidirectionally under nutrient-limited conditions, but preferentially stall under nutrient-supplemented conditions. Motility types correlate with subcellular localisation of FimX, a protein required for TFP assembly and implicated in environmental response. The subcellular distribution of FimX is asymmetric for unidirectional crawling, consistent with TFP assembled primarily at the leading pole, whereas for non-translational types FimX expression is symmetric or non-existent. These results are consistent with a minimal stochastic model that reproduces the motility types from the subcellular average concentration and asymmetry of FimX. These findings reveal that P. aeruginosa deploy TFP symmetrically or asymmetrically to modulate motility behaviours in different nutrient conditions and thereby form biofilms only where nutrients are sufficient, which greatly enhances their competitive capacity in diverse environments.