Bacteria Tune a Trade-off between Adhesion and Migration to Colonize Surfaces under Flow

Abstract

The bacterial colonization of surfaces is a ubiquitous process that shapes nature and profoundly affects human health. While much is known about the biology of this process, the pivotal interplay between physical environment and active bacterial micromechanics remains poorly understood. In fact, strong adhesion and high motility, both of which are essential for surface colonization, are two apparently contradictory goals, as they mutually obstruct each other. Here, we investigate how the human pathogen Pseudomonas aeruginosa optimizes its behavior for colonization of surfaces under flow. From the analysis of the dynamics of fluorescently labeled type-IV pili, we construct a mathematical model that quantitatively connects individual motor dynamics with whole-cell motility and migration. The data analysis also reveals that cells upregulate the number of visible pili on surface contact, although individual pili do not display a measurable sensory response to surfaces. When applying shear flow, we unexpectedly find that robust sticking to a surface requires passive surface adhesion rather than pilus activity. Instead, pilus activity actually promotes cell detachment while enabling migration. Using genetic perturbations of the pilus apparatus, it is shown that wild-type cells achieve a trade-off between adhesion and migration by limiting the number of pili. Simulations reveal a generic underlying trait space, where, depending on the interplay of active and passive forces, adhesion and migration are either compatible or a trade-off is required for efficient bacterial surface colonization. The discovered adhesion-migration problem is paradigmatic of a broad class of piliated bacteria and may also have implications for other cells.