A Skeptic's Guide to Bacterial Mechanosensing

Abstract

Surface sensing in bacteria is a precursor to the colonization of biotic and abiotic surfaces, and an important cause of drug resistance and virulence. As a motile bacterium approaches and adheres to a surface from the bulk fluid, the mechanical forces that act on it change. Bacteria are able to sense these changes in the mechanical load through a process termed mechanosensing. Bacterial mechanosensing has featured prominently in recent literature as playing a key role in surface sensing. However, the changes in mechanical loads on different parts of the cell at a surface vary in magnitudes as well as in signs. This confounds the determination of a causal relationship between the activation of specific mechanosensors and surface sensing. Here, we explain how contrasting mechanical stimuli arise on a surface-adherent cell and how known mechanosensors respond to these stimuli. The evidence for mechanosensing in select bacterial species is reinterpreted, with a focus on mechanosensitive molecular motors. We conclude with proposed criteria that bacterial mechanosensors must satisfy to successfully mediate surface sensing.

Keywords: Appendages; Motility; Motors; Surface-sensing; Viscous load.

Figure 1.

A) A swimmer experiences a persistent viscous drag force (F_Drag) and a resistive torque (τ_Drag) due to its motility (top). When it encounters a surface that obstructs its motility, it immediately experiences a reduction in F_Drag and τ_Drag in a quiescent fluid. B) The pre-stimulus load on the cell body is proportional to the swimming speed and the cell’s counter-rotation frequency. Attachment to a surface causes a negative change in load: ΔF_Drag ~ −1 pN, and Δτ_Drag ~ −1600 pN nm.

Figure 2

A) Scenario I – cell body is surface-attached but the appendages are free and unloaded. Scenario II – the cell and prominent appendages become surface-attached and thus, loaded. B) Flagellar attachment to the surface will cause a rotation of the cell provided other appendages remain unattached. C) Cases where cell may attach to a surface due to the presence of adhesive components on its body, and is able to freely-pivot around the joint. Cell rotation occurs either due to hydrodynamic interactions of the rotating flagellum with the surface (left) or due to off-axis flagellar thrust that generates a torque on the cell (right). Another possibility is that the cell simply counter-rotates around the fluid joint due to on-axis flagellar rotation. D) and E) Increase in flagellar and pili-loads when the respective appendages attach to the surface and are stalled, as indicated in scenario II.

Figure 3

A) Top: The contact area between the surface and the attached cell is a tiny fraction of the overall surface area of the cell (top view). The adhesion forces act only on this area. Bottom: In a non-quiescent fluid, the tensile force on a surface-adherent pilus is a combination of the shear force, the adhesion force, and the retractile force. When the fluid flow is in a direction opposite to the retractile force, it reduces the total tensile force. B) An attached cell viewed along its pole. Top: the un-deformed cell diameter is a. Inactive putative mechanosensitive channels embedded within the cell membrane are indicated in the inset figures. Bottom: The cell deforms over a period of time to h, and the channels along the top and side sections of the cell experience contrasting forces as indicated by the arrows in the inset.