Asymmetric adhesion of rod-shaped bacteria controls microcolony morphogenesis

Abstract

Surface colonization underpins microbial ecology on terrestrial environments. Although factors that mediate bacteria–substrate adhesion have been extensively studied, their spatiotemporal dynamics during the establishment of microcolonies remains largely unexplored. Here, we use laser ablation and force microscopy to monitor single-cell adhesion during the course of microcolony formation. We find that adhesion forces of the rod-shaped bacteria Escherichia coli and Pseudomonas aeruginosa are polar. This asymmetry induces mechanical tension, and drives daughter cell rearrangements, which eventually determine the shape of the microcolonies. Informed by experimental data, we develop a quantitative model of microcolony morphogenesis that enables the prediction of bacterial adhesion strength from simple time-lapse measurements. Our results demonstrate how patterns of surface colonization derive from the spatial distribution of adhesive factors on the cell envelope.

Bacteria as living patchy colloids: Phenotypic heterogeneity in surface adhesion

“…When initial adhesion leads to the formation of a full-blown biofilm, different adhesive proteins are involved in binding cells to the substrate or to each other ( 10 , 49 ). Both population variations in adhesion strength ( 50 ) and the location on the cell surface of adhesive interactions ( 51 ) are of importance. The study of a variety of organisms under diverse conditions will therefore be needed to establish a full picture.…”

Geometry and Mechanics of Microdomains in Growing Bacterial Colonies

“…We stress here that our approach does not aim to faithfully reproduce all the experimental details but rather to provide a conceptual key for understanding certain geometrical and mechanical properties, with the help of a minimal model comprising a single fitting parameter: i.e., the timescale τ = ζ/Y . Other properties, such as the roughness of the colony edge and smoother variation in the orientation of neighboring domains, are not well captured by our simple model and would require a more sophisticated construction, accounting for the adhesive interaction between neighboring cells, the flexibility of the cell membrane, and more specific cell-substrate interactions [31]. Unfortunately, this would imply a cost in terms of free parameters and reduced simplicity in the interpretation of the numerical results.…”

Clustering of bacteria with heterogeneous motility

“…Focusing on the dynamics at the particle scale, the balance between nucleation-division and diffusion-aggregation processes shall control the emergence of microcolonies [14][15][16][17]. For example, motility can either favor bacterial aggregation by enabling cell-cell encounters [15] but also prevent localized aggregates by enhancing dispersion [18].…”