Effects of prey quality through the life cycle of the social amoeba Dictyostelium discoideum

Generalist consumers can eat a variety of foods, but they are not necessarily equally beneficial. Different feeding histories can influence the fitness of genetically similar individuals. Dictyostelium discoideum is a unicellular generalist predator amoeba that eats bacteria. When bacteria are depleted, amoebae enter the social cycle and aggregate to form a fruiting body, in which about a fifth of the amoebae die to form a stalk while the rest form spores at the top of the stalk. In this study, we examined the fitness of D. discoideum when grown on three bacterial prey types: poorly palatable wild-type Pseudomonas vindicans, a more palatable mutant of the same species, and the high-quality food bacterium Klebsiella pneumoniae. We used these three bacteria to examine how feeding history shapes fitness throughout the life cycle by measuring proliferation of amoebae, then following spores through germination, plaque formation, and plaque expansion. Amoebae grew on unpalatable P. vindicans only when seeded at high density, and even then, proliferated more slowly. When amoebae with different feeding histories were mixed and allowed to form chimeric fruiting bodies, those cells fed on palatable versus unpalatable P. vindicans did not differ significantly in their spore contribution, except when under an additional stress of the translational inhibitor G418, which makes cells that previously fed on unpalatable P. vindicans contribute fewer cells in spores. Oddly, the amoebae that fed on the good food bacterium Klebsiella pneumoniae contributed fewer spores when mixed with cells that fed on either of the P. vindicans clones. Surprisingly, though feeding on unpalatable prey was not a hindrance in the social stage, downstream effects were observed. Spores produced on either P. vindicans strain germinated more slowly than those made from amoebae fed on Klebsiella pneumoniae. Low prey quality strongly affects D. discoideum fitness during the vegetative stage but does not generally lower social competitive ability. Nevertheless, it does affect fitness after the social cycle by reducing the hatching rate of spores.