The Onset of Collective Behavior in Social Amoebae

All Together Now In the social amoeba Dictyostelium discoideum, periodic synthesis and release of cyclic AMP (cAMP) guides the cellular aggregation required to form fruiting bodies. It has been unclear whether the initiation of this behavior is owing to synchronization of autonomously oscillating cells or whether individual cells remain nonoscillatory unless the entire population becomes oscillatory. Gregor et al. (p. 1021, published online 22 April; see the Perspective by Prindle and Hasty) used live-cell imaging to show that cAMP pulses originate from a specific location in space and that individual cells move in and out of these signaling centers. The observations suggest that oscillations do not originate from autonomous activities of specialized cells. However, individual cells do display stochastic cAMP-pulsing below a threshold external concentration of cAMP, and the generation of synchronized oscillations could only be modeled accurately when this random pulsing was taken into account. Stochastic pulsing of individual cells plays a critical role in initiating cyclic adenosine monophosphate pulses. In the social amoebae Dictyostelium discoideum, periodic synthesis and release of extracellular cyclic adenosine 3′,5′-monophosphate (cAMP) guide cell aggregation and commitment to form fruiting bodies. It is unclear whether these oscillations are an intrinsic property of individual cells or if they exist only as a population-level phenomenon. Here, we showed by live-cell imaging of intact cell populations that pulses originate from a discrete location despite constant exchange of cells to and from the region. In a perfusion chamber, both isolated single cells and cell populations switched from quiescence to rhythmic activity depending on the concentration of extracellular cAMP. A quantitative analysis showed that stochastic pulsing of individual cells below the threshold concentration of extracellular cAMP plays a critical role in the onset of collective behavior.

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