Figure 1.
Schematics of alternative mechanisms of gliding motility and their representation in biophysical models of the M. xanthus cell.
(A) Focal adhesion mechanism (FAM) - Multi-protein complexes (green bars) spanning from the cytoplasm to the outside of the cell attach to the underlying substrate at specific points. Cells move forward as a result of the force generated by the components of these complexes against cytoskeleton (B) Helical rotor mechanism (HRM) - Motor proteins (green dots) tracking on a helical cytoskeleton create distortions in cell wall. These distortions generate drag forces between the substrate and the cell surface and result in cell movement. (C) Distinctions in cell-substrate interactions for the two alternative models of gliding motility. In the elastic coupling model during a cell-cell collision, a restoration force acts on the cell at the cell-substrate interaction points (green dots) in the direction perpendicular to cell axis. No such force exists in the viscous coupling model.
Figure 2.
Mechanical interactions between two cells during head-to-side collisions in the biophysical models and experiments.
(A) Viscous coupling model – both cells change directions. (B) Elastic coupling model – only the secondary cell changes direction. (C) Experimental time-lapse images (rotated to match with simulation configuration) showing collision between two isolated cells where only the secondary cell changes its direction. See videos S1, S2, S3 for corresponding movies.
Figure 3.
Strong adhesive attachments between cell and substrate are required to match experimental observations.
(A) Maximum change in primary cell orientation () as a function of the strength of substrate attachments (
). Red band represents the range of bond strengths observed for integrin bonds in other biological systems (22–24). Horizontal solid line (
) represents the mean value of change in primary cell orientation from experimental cell collisions after subtracting the spontaneous cell turning and the dashed lines represent one standard deviation variation in the experimental data. (B) Same as (A) but with mean and standard deviation from aggregated simulations with varied model parameters. (C) The minimum adhesive strength of attachments matching experimental data closely matches with the cell propulsion force. Error bars represent variation in the results for different cell flexibilities. (D) The distribution of
values in experimental data of wild-type cells (DK1622, collision events, N = 97) and (E) cells lacking twitching motility (DK10407, N = 58). (F) The distribution of spontaneous cell orientation change for mean cell collision time of ∼2.9 min measured from trajectories of isolated cells (DK1622, N = 4018, see Fig. S4A for additional details).
Figure 4.
Distinct cell behavior from the two cell models for variation in collision geometries.
(A) The change in primary cell orientation () as a function of collision position from the leading end of the primary cell and (B) as a function of collision angle.
Figure 5.
Bead/molecular motor motility behavior under optical trap loading.
(A) A gliding motor moves a bead along the cell axis. Past a preset threshold movement, the shutter in front of the optical trap is opened, pulling the bead in the direction opposite to the motor by the preset force, resulting in a slowing of bead movement. (B–D) For opposing forces of 12 pN or greater (18 pN) bead movement has stopped and for lower forces (9 pN) bead movement is slowed down but not completely stopped. Here an experiment is associated with the activity of a single motor only if the bead moves before and after trapping with the same direction and speed (green lines). A linear fit to the position versus time during force application provides the velocity (blue lines). (E) Bead velocity decreases exponentially with force but never becomes negative consistent with an elastic coupling and inconsistent with a viscous coupling between the bead and motor. The dashed lines are an exponential fit to the data. Error bars represent the standard error of the mean across trials (>6 trials per data point). (F) Force-velocity curves normalized by unloaded velocity corresponding to different nigericin concentrations (blue circles – 0 µM, brown circles – 10 µM, red circles – 20 µM; see Fig. S6 for individual curves) collapse on to a single line on a semi-log plot.