Flow-induced bending of flagella restricts Pseudomonas aeruginosa surface departure

Shear force associated with flow can bend, twist, or stretch cellular appendages. Bacterial appendages such as flagella can rotate and generate forces. However, it is unclear how environmental and cell-generated forces interact as bacteria associate with surfaces. Here, we use microfluidics, flagellar labeling, and genetics to discover that flow bends flagella to restrict surface departure of the human pathogen Pseudomonas aeruginosa. By imaging wild-type cells with blocked flagella and using mutants with paralyzed flagella, we demonstrate that flagellar rotation force promotes surface departure in host-relevant shear regimes. Our single-cell experiments reveal two distinct subpopulations in flow: cells with their flagellum positioned upstream and cells with their flagellum positioned downstream. By independently modulating flow and solution viscosity, we show that shear force bends upstream flagella around the cell and blocks rotation within seconds after surface arrival. In contrast, downstream flagella can continue to rotate after surface arrival. Cells with downstream flagella depart the surface more frequently than cells with upstream flagella, indicating how flow direction can determine bacterial cell fate on surfaces. Together, our results demonstrate how the geometric relationship between flow and cell appendages can generate subpopulations and control surface behaviors.

Bacteria use cell appendages such as flagella to interact with their environment. While bacteria are typically studied in conditions that lack flow, host environments are often flowing. In this study, we use microfluidic devices to test how host-relevant flow impacts flagella of the human pathogen Pseudomonas aeruginosa. As each P. aeruginosa cell has only one flagellum, we observed cells with their flagellum facing upstream and cells with their flagellum facing downstream. We discover that while shear force bends upstream flagella and prevents their rotation, downstream flagella can continue to rotate. As a consequence, cells with downstream flagella are more likely to depart the surface. Our results reveal a mechanism by which shear force can impact the surface behavior of a bacterial pathogen.