Bacteria use type-IV pili to slingshot on surfaces

Abstract

Bacteria optimize the use of their motility appendages to move efficiently on a wide range of surfaces prior to forming multicellular bacterial biofilms. The "twitching" motility mode employed by many bacterial species for surface exploration uses type-IV pili (TFP) as linear actuators to enable directional crawling. In addition to linear motion, however, motility requires turns and changes of direction. Moreover, the motility mechanism must be adaptable to the continually changing surface conditions encountered during biofilm formation. Here, we develop a novel two-point tracking algorithm to dissect twitching motility in this context. We show that TFP-mediated crawling in Pseudomonas aeruginosa consistently alternates between two distinct actions: a translation of constant velocity and a combined translation-rotation that is approximately 20× faster in instantaneous velocity. Orientational distributions of these actions suggest that the former is due to pulling by multiple TFP, whereas the latter is due to release by single TFP. The release action leads to a fast "slingshot" motion that can turn the cell body efficiently by oversteering. Furthermore, the large velocity of the slingshot motion enables bacteria to move efficiently through environments that contain shear-thinning viscoelastic fluids, such as the extracellular polymeric substances (EPS) that bacteria secrete on surfaces during biofilm formation. extracellular polysaccharides | cystic fibrosis | biometric identification | PAO1 B acterial biofilms are multicellular communities that adhere to almost any surface and are fundamental to the ecology and biology of bacteria (1). To assemble into microcolonies and form biofilms, bacteria must adapt their motility mechanisms for surface locomotion (2, 3). For example, both flagella (4) and excreted surfactants (5) enable collective surface motility modes (6, 7) that allow bacteria to colonize surfaces. Many bacterial species, including the opportunistic pathogen Pseudomonas aeruginosa, which contributes to fatal airway infections in cystic fibrosis (8, 9), the causative agent for gonorrhea Neisseria gonorrhoeae, and the predatory soil bacterium Myxococcus xanthus (10), use type-IV pili (TFP) to move on surfaces (11)(12)(13)(14)(15). TFP are associated with the "twitching" collective motility mode (16), in which cells exhibit apparently random irregular motions. A single type-IV pilus undergoes cycles of repeated extensionadhesion and retraction-release (17, 18) that are driven by an ATP motor (19,20). Single TFP can generate forces of up to approximately 100 pN (21, 22), and multiple pili can cooperatively generate forces of up to approximately 1 nN (23), to enable motion on surfaces. To traverse distances that are significantly longer than the extension distance of a single pilus (typically several microns) (17), bacteria deploy multiple pili using a "tug-of-war" mechanism (24). These studies show that TFP act as linear actuators (17) to enable directional motion.What is not known is how the collective dep...

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