Simulated Heat Waves Affect Cell Fate and Fitness in the Social Amoeba Dictyostelium discoideum

The effects of heatwaves at organism and population levels have been widely investigated; however, little is known about how they affect the development of cell populations and the fitness of the resulting organism. Disruptions caused by heatwaves are especially critical during early developmental stages in organisms lacking parental developmental protection or care. Here we use the social amoeba Dictyostelium discoideum, a soil microbe with a life cycle that transitions between single-cell and multicellular stages. D. discoideum thrives optimally at 22 °C and elevated temperatures impair (27 °C) or completely arrest (30 °C) growth, development, and spore yield. We established a simulated heatwave model in which vegetative cells were exposed to 27 °C for 3 days and studied the effects on the expression of early and cell type specific developmental genes using real-time quantitative PCR. A single heatwave severely impaired the expression of cyclic AMP-dependent early developmental gene markers (carA, acaA, pkaR, gtaC, tgrC1, and csaA) as well as that of prespore markers (cotB and spiA), while the expression of the prestalk marker ecmA was less affected. When mixed with heat-stressed cells, reporter cells expressing β-galactosidase grown at 22 °C preferentially occupy the spore mass of the fruiting body. Chimera assays of wild-type and reporter cells grown at optimal temperature or subjected to a heatwave confirmed a decreased fitness (contribution to chimeric fruiting bodies). We conclude that exposure of unprotected organisms at the single cell stage to a single heatwave has the potential to negatively impact their ability to cope with environmental extremes.