Spiral and concentric waves organize multicellular Dictyostelium mounds

Abstract

It has been known for more than 20 years that the early aggregation of the slime mould Dictyostelium is driven by periodic waves of cAMP, which instruct the cells to collect at the aggregation centre. Although it has been hypothesized that cAMP waves are also involved in the organization of multicellular morphogenesis, wave propagation in the later stages of Dictyostelium development has not previously been demonstrated. We have developed special optical and digital-image-processing techniques that allow propagating waves of chemotactic activity to be visualized in multicellular aggregates. Using this technology, we have observed signal propagation in the multicellular, 'mound' stage of Dictyostelium discoideum. Within mounds, these waves were propagated as concentric rings, single armed spirals or multi-armed spirals. The spontaneous appearance of the latter structures was new and unexpected. The geometry of wave propagation was strain specific: strain XP55 predominantly showed concentric ring waves, whereas spiral waves were typical of a derivative of XP55, streamer F mutant NP377, and of the widely used axenic strain AX-3. The different geometry of the signals was reflected by distinct cell-movement patterns and different cell-movement speeds--cells in AX-3 mounds, organized by spiral waves, moved faster than cells in XP55 mounds, and spiral waves were always accompanied by rotational cell movement, whereas cells in XP55 mounds moved towards the aggregation centre. The same principles--wave propagation and chemotaxis--that control Dictyostelium aggregation also govern the morphogenesis of the mound stage. Mounds behave as a highly excitable system in which a diverse range of signal-propagation geometries create the same biological structure--a migrating slug.