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

Cyanobacteria are key contributors to biogeochemical cycles through photosynthesis and carbon fixation. In filamentous, multicellular cyanobacteria, these functions can be influenced through gliding motility, which enables filaments to localise in response to light and also form aggregates. Here, we use the aggregate-forming species <i>Fluctiforma draycotensis</i> to study gliding motility dynamics in detail. We find that filaments move in curved and straight trajectories interspersed with reorientation or reversal of direction. Most reversals take a few seconds, but some take substantially longer, resulting in a long-tailed distribution of stoppage times. Mean filament speeds range around a micron per second with a relatively uniform distribution against filament length, implying that all or a fixed proportion of cells in a filament contribute to movement. We implement a biophysical model that can recapitulate these findings. Model simulations show that for filaments to reverse quickly, cells in a filament must achieve high coordination of the direction of the forces that they generate. To seek experimental support for this prediction, we track individual cells in a filament. This reveals that cells' translational movement is fully coupled with their rotation along the long axis of the filament, and that cellular movement remains coordinated throughout a reversal. For some filaments, especially longer ones, however, we also find that cellular coordination can be lost, and filaments can form buckles that can twist around themselves, resulting in plectonemes. The experimental findings and the biophysical model presented here will inform future studies of individual and collective filament movement.