Myxococcus xanthus Gliding Motors Are Elastically Coupled to the Substrate as Predicted by the Focal Adhesion Model of Gliding Motility

Abstract

Myxococcus xanthus is a model organism for studying bacterial social behaviors due to its ability to form complex multi-cellular structures. Knowledge of M. xanthus surface gliding motility and the mechanisms that coordinated it are critically important to our understanding of collective cell behaviors. Although the mechanism of gliding motility is still under investigation, recent experiments suggest that there are two possible mechanisms underlying force production for cell motility: the focal adhesion mechanism and the helical rotor mechanism, which differ in the biophysics of the cell–substrate interactions. Whereas the focal adhesion model predicts an elastic coupling, the helical rotor model predicts a viscous coupling. Using a combination of computational modeling, imaging, and force microscopy, we find evidence for elastic coupling in support of the focal adhesion model. Using a biophysical model of the M. xanthus cell, we investigated how the mechanical interactions between cells are affected by interactions with the substrate. Comparison of modeling results with experimental data for cell-cell collision events pointed to a strong, elastic attachment between the cell and substrate. These results are robust to variations in the mechanical and geometrical parameters of the model. We then directly measured the motor-substrate coupling by monitoring the motion of optically trapped beads and find that motor velocity decreases exponentially with opposing load. At high loads, motor velocity approaches zero velocity asymptotically and motors remain bound to beads indicating a strong, elastic attachment.

Author Summary

Studies of collective bacterial motility on solid surfaces are essential for understanding self-organization of biofilms. The Gram-negative bacterium Myxococcus xanthus has long been used as a model organism for studying surface motility but its mechanism of gliding is still under investigation. Recent experiments point to two potential mechanisms for gliding motility that differ qualitatively in the details of their cell-substrate interactions. To investigate the biophysical nature of this interaction (viscous vs. elastic coupling), we developed a synergistically multidisciplinary approach combining computational modeling, time-lapse microscopy, and biophysical optical trap experiments. First we studied the mechanical cell interaction behavior in isolated cell pair collisions in a computational model and compared the results with experimental cell behavior. The results indicated a strong adhesive attachment between cell and substrate which is further confirmed by applying opposing loads on beads attached to cell surface in an optical trap. Thus our results conclusively showed strong adhesive attachments between cell and substrate, providing support for an elastic rather than viscous coupling between cell and substrate similar to phenomena observed in focal adhesions from eukaryotic cells.