It is critical for bacteria to recognize surface contact and to initiate physiological changes required for surface-associated lifestyles. Ubiquitous microbial appendages called pili are involved in sensing surfaces and mediating downstream behaviors, but the mechanism by which pili mediate surface sensing remains unclear. Here we visualized Caulobacter crescentus pili undergoing dynamic cycles of extension and retraction. These cycles ceased within seconds of surface contact, which coincided with synthesis of the adhesive holdfast required for attachment. Physically blocking pili imposed resistance to pilus retraction, which was sufficient to stimulate holdfast synthesis without surface contact. Thus, resistance to pilus retraction upon surface contact is used for surface sensing.

One Sentence Summary: Bacteria use the tension imparted on retracting pilus fibers upon their binding to a surface for surface sensing. Abstract:Surface association provides numerous fitness advantages to bacteria. Thus, it is critical for bacteria to recognize surface contact and to consequently initiate physiological changes required for a surface-associated lifestyle (1). Ubiquitous microbial appendages called pili are involved in sensing surfaces and mediating downstream surface-associated behaviors (2-6). The mechanism by which pili mediate surface sensing remains unknown, largely due to the difficulty to visualize their dynamic nature and to directly modulate their activity without genetic modification. Here, we show that Caulobacter crescentus pili undergo dynamic cycles of extension and retraction that cease within seconds of surface contact, and this arrest of pilus activity coincides with surface-stimulated holdfast synthesis. By physically blocking pili, we show that imposing resistance to pilus retraction is sufficient to stimulate holdfast synthesis in the absence of surface contact. Thus, resistance to type IV pilus retraction upon surface attachment is used for surface sensing.

16Molecular motors convert chemical energy directly into mechanical work 1 and are found in all 17domains of life 2 . These motors are critical to intracellular transport 3 , motility 4,5 , macromolecular 18protein assembly 3,6 , and many essential processes 7 . A wide-spread class of related bacterial 19 motors drive the dynamic activity of extracellular fibers, such as type IV pili (T4P), that are 20 extended and retracted using so-called secretion motor ATPases. Among these, the tight 21 adherence (tad) pili are critical for surface sensing, surface attachment, and biofilm formation 8-22 10