Mechanical limitation of bacterial motility mediated by growing cell chains

Contrasting most known bacterial motility mechanisms, a bacterial sliding motility discovered in at least two gram-positive bacterial families does not depend on designated motors. Instead, the cells maintain end-to-end connections following cell divisions to form long chains and exploit cell growth and division to push the cells forward. To investigate the dynamics of this motility mechanism, we constructed a mechanical model that depicts the interplay of the forces acting on and between the cells comprising the chain. Due to the exponential growth of individual cells, the tips of the chains can, in principle, accelerate to speeds faster than any known single-cell motility mechanism can achieve. However, analysis of the mechanical model shows that the exponential acceleration comes at the cost of an exponential buildup in mechanical stress in the chain, making overly long chains prone to breakage. Additionally, the mechanical model reveals that the dynamics of the chain expansion hinges on a single non-dimensional parameter. Perturbation analysis of the mechanical model further predicts the critical stress leading to chain breakage and its dependence on the non-dimensional parameter. Finally, we developed a simplistic population-expansion model that uses the predicted breaking behavior to estimate the physical limit of chain-mediated population expansion. Predictions from the models provide critical insights into how this motility depends on key physical properties of the cell and the substrate. Overall, our models present a generically applicable theoretical framework for cell-chain-mediated bacterial sliding motility and provide guidance for future experimental studies on such motility.