Pattern formation by a cell surface-associated morphogen in Myxococcus xanthus

Abstract

In response to starvation, an unstructured population of identical Myxococcus xanthus cells rearranges into an asymmetric, stable pattern of multicellular fruiting bodies. Central to this pattern formation process are changes in organized cell movements from swarming to aggregation. Aggregation is induced by the cell surface-associated C-signal. To understand how aggregation is accomplished, we have analyzed how C-signal modulates cell behavior. We show that C-signal induces a motility response that includes increases in transient gliding speeds and in the duration of gliding intervals and decreases in stop and reversal frequencies. This response results in a switch in cell behavior from an oscillatory to a unidirectional type of behavior in which the net-distance traveled by a cell per minute is increased. We propose that the C-signal-dependent regulation of the reversal frequency is essential for aggregation and that the remaining C-signal-dependent changes in motility parameters contribute to aggregation by increasing the net-distance traveled by starving cells per minute. In our model for symmetry-breaking and aggregation, C-signal transmission is a local event involving direct contacts between cells that results in a global organization of cells. This pattern formation mechanism does not require a diffusible substance or other actions at a distance. Rather it depends on contact-induced changes in motility behavior to direct cells appropriately

Figure 1

Motility parameters of wt and csgA cells during development. The data in the first, second, and third columns were collected at 3, 9, and 15 h, respectively. (a, e, and i) Gliding speed profiles of representative wt cells developed in the context of other wt cells. Each panel shows the speed profile of a single representative cell. The dotted lines indicate the detection limit for active movement. A reversal is a change in speed from a positive to a negative value, or vice versa. (b, f, and j) Gliding speed profiles of representative csgA cells developed in the context of other csgA cells. Each panel shows the speed profile of a single representative cell. The dotted lines indicate the detection limit for active movement. A reversal is a change in speed from a positive to a negative value, or vice versa. (c, g, and k) Distributions of transient gliding speeds in wt cells developed in the context of other wt cells and csgA cells developed in the context of other csgA cells. Each distribution was prepared from at least 1,180 transient gliding speeds calculated from at least 20 cells. (d, h, and i) The x,y positions of representative wt cells developed in the context of other wt cells and csgA cells developed in the context of other csgA cells. Each trajectory represents the x,y positions of a representative cell as recorded every 15 s during a recording period of 900 s.