Cellular (de)coordination in gliding motility and plectoneme formation

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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.

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Significance Statement

Gliding motility is seen in diverse bacteria, but the dynamics of this type of motion and the molecular mechanisms creating propulsive forces are still not fully understood. In some gliding cyanobacteria, many cells remain attached to each other to form a single filament, thus necessitating an intra-cellular coordination of propulsive forces. To better understand such coordination, we study here the dynamics of gliding motility in a filamentous cyanobacteria. We find that, on agar surface, gliding filaments move back-and-forth in a well-defined trajectory and their translation is coupled with rotation along the long axis of the filament. During reversals, cells mostly remain coordinated with each other. These dynamics are captured by a physical model, which predicts that a loss of cell-to-cell coordination can cause loss of smooth reversal. Confirming this prediction, we find that longer filaments can readily get de-coordinated during reversals, resulting in the buckling of filaments and formation of plectonemes. These experimental results and the developed model will inform future studies of molecular mechanisms in single filaments and collective behaviors of many filaments.