ATP levels influence cell movement during the mound phase in Dictyostelium discoideum as revealed by ATP visualization and simulation

Abstract

Cell migration plays an important role in multicellular organism development. The cellular slime mold Dictyostelium discoideum is a useful model organism for the study of cell migration during development. Although cellular ATP levels are known to determine cell fate during development, the underlying mechanism remains unclear. Here, we report that ATP‐rich cells efficiently move to the central tip region of the mound against rotational movement during the mound phase. A simulation analysis based on an agent‐based model reproduces the movement of ATP‐rich cells observed in the experiments. These findings indicate that ATP‐rich cells have the ability to move against the bulk flow of cells, suggesting a mechanism by which high ATP levels determine the cell fate of differentiation.

Single-cell phenotypic plasticity modulates social behaviour inDictyostelium discoideum

“…As amoebae crawl by extending pseudopods (Kessin, 2001), variations in adhesion to the substratum may alter the probability of aggregation by altering the speed of displacement. This hypothesis is supported by numerical models for binary mixes of self-propelled particles, that showed that differential motility can result into assortment within the aggregated phase (Forget et al, 2022; Kolb and Klotsa, 2020; S. Punla et al, 2022).Moreover, cell motility has been recently invoked as the basis of differentiation biases observed in cells with different intracellular ATP concentration (Hiraoka et al, 2020, 2022). We measured individual cell motility in populations harvested in EE, ME, LE, and ES phase.…”

“…Cell-surface attachment, cell-cell adhesion and single-cell motility all show related changes during the initial phases of culture growth. We focused in particular on characterizing variation in the distribution of single-cell motility because, on the one hand, motility appears to be regulated by ATP independently from cAMP oscillations (Hiraoka et al, 2022). On the other hand, it can be connected more directly to the observed increase in proportion of aggregated cells as the growth phase advances.…”

Single-cell phenotypic plasticity modulates social behavior in Dictyostelium discoideum

“… 24 , 53 Moreover, cell motility has been recently invoked as the basis of differentiation biases observed in cells with different intracellular ATP concentration. 44 , 54 We measured individual cell motility in populations harvested in EE, ME, LE, and ES phase.…”

“…We focused in particular on characterizing variation in the distribution of single-cell motility because, on one hand, motility appears to be regulated by ATP independently from cyclic adenosine monophosphate (cAMP) oscillations. 54 On the other hand, it can be connected more directly to the observed increase in proportion of aggregated cells as the growth phase advances. When a population ages, indeed, the fraction of actively dividing cells (in the M phase of the cell cycle) is known to decrease.…”