Cellular coordination underpins rapid reversals in gliding filamentous cyanobacteria and its loss results in plectonemes

Abstract

Gliding motility involves a characteristic back-and-forth movement of cells without flagella, and is seen in diverse bacteria. It is currently unknown how reversal dynamics in gliding motility are coordinated, especially in the case of multi-cellular, filamentous cyanobacteria. Here, we study gliding motility dynamics in a recently described species, capable of extensive gliding motility and collective, macro-structure formation. We find that gliding motility involves filaments rotating and translating through slime tubes, rather than on top of slime. On agar, filaments move back-and-forth on well-defined trajectories, where they display a characteristic speed profile, peaking in the middle of the trajectory. The time spent during each reversal displays a long-tailed distribution, with most reversals being almost instantaneous, while few involve a significant time of no movement. During reversals, individual cells remain mostly coordinated in their motion. Based on these experimental observations, we develop a biophysical model that incorporates cellular propulsive forces, the direction of which is decided by each cell based on mechano-sensing of their neighbors' motion. This model can capture experimental observations and predicts that loss of mechano-sensing can cause de-coordination of filament ends during reversals. In line with this prediction, we find instances of filaments becoming de-coordinated during reversals and that these instances are associated with plectoneme formation. The presented characterisation of filament movement dynamics and the corresponding physical model will inform future studies on individual and collective filament behaviours under different conditions.