Abstract
Type IV pili are ubiquitous bacterial motors that power surface motility. In peritrichously piliated species, it is unclear how multiple pili are coordinated to generate movement with directional persistence. Here we use a combined theoretical and experimental approach to test the hypothesis that multiple pili of Neisseria gonorrhoeae are coordinated through a tug-of-war. Based on force-dependent unbinding rates and pilus retraction speeds measured at the level of single pili, we build a tug-of-war model. Whereas the one-dimensional model robustly predicts persistent movement, the two-dimensional model requires a mechanism of directional memory provided by re-elongation of fully retracted pili and pilus bundling. Experimentally, we confirm memory in the form of bursts of pilus retractions. Bursts are seen even with bundling suppressed, indicating re-elongation from stable core complexes as the key mechanism of directional memory. Directional memory increases the surface range explored by motile bacteria and likely facilitates surface colonization.
Highlights
Type IV pili are ubiquitous bacterial motors that power surface motility
Twitching is a mechanism for bacterial motility along a surface driven by type IV pili[16,17,18,19,20], micron-sized polymeric cell appendages that play a role in motility and in cell–cell adhesion, cell-surface adhesion and horizontal gene transfer[20,21,22]
The coordination of multiple pili depends on the where pili are located on the cell surface and appears to be different in different bacterial species
Summary
Type IV pili are ubiquitous bacterial motors that power surface motility. In peritrichously piliated species, it is unclear how multiple pili are coordinated to generate movement with directional persistence. In M. xanthus it has been shown that the presence of pili at the poles is dynamically regulated through the localized activation of the assembly system (which itself has recently been shown to be stable and remain at both poles29) and clustering of the PilT and PilB proteins, two antagonistic ATPases promoting pilus retraction and elongation, respectively[28] In both species, the patterns of motion can be complex with several modes of pili-dependent motility in P. aeruginosa[30,31] and both pilidependent and pili-independent mechanisms of surface motility in M. xanthus[32]. No biochemical mechanism coordinating their retraction is known, yet the quantitative analysis of bacterial trajectories provides clear evidence for the cooperation of multiple pili[15] These observations suggested that the coordination of multiple pilus motors may be mediated mechanically via a tug-of-war of pilus motors pulling in different directions[15]. Diplococci (pairs of bacteria) were observed to align and meander in micro-topographic grooves, Cell body
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