Abstract
The social amoeba Dictyostelium discoideum is widely studied for its multicellular development program as a response to starvation and constitutes a model of choice in microbial cooperation studies. Aggregates of up to 10 (6) cells form fruiting bodies containing two cell types: (i) dormant spores (~80%) that can persist for months in the absence of nutrients, and (ii) dead stalk cells (~20%) that promote the dispersion of the spores towards nutrient-rich areas. It is often overlooked that not all cells aggregate upon starvation. Using a new quantitative approach based on time-lapse fluorescence microscopy and a low ratio of reporting cells, we have quantified this fraction of non-aggregating cells. In realistic starvation conditions, up to 15% of cells do not aggregate, which makes this third cell fate a significant component of the population-level response of social amoebae to starvation. Non-aggregating cells have an advantage over cells in aggregates since they resume growth earlier upon arrival of new nutrients, but have a shorter lifespan under prolonged starvation. We find that phenotypic heterogeneities linked to cell nutritional state bias the representation of cells in the aggregating vs. non-aggregating fractions, and thus regulate population partitioning. Next, we report that the fraction of non-aggregating cells depends on genetic factors that regulate the timing of starvation, signal sensing efficiency and aggregation efficiency. In addition, interactions between clones in mixtures of non-isogenic cells affect the partitioning of each clone into both fractions. We further test the evolutionary significance of the non-aggregating cell fraction. The partitioning of cells into aggregating and non-aggregating fractions is optimal in fluctuating environments with an unpredictable duration of starvation periods. D. discoideum thus constitutes a model system lying at the intersection of microbial cooperation and bet hedging, defining a new frontier in microbiology and evolution studies.
Highlights
Every organism has a set of optimal conditions that maximizes its fitness
When we plated a population of genetically identical axenic wildtype AX3 cells of D. discoideum on nutrient-free substrates at a 104–107 cells/cm[2] density range[21], we observed that some cells aggregate while others remain outside of aggregates (Figure 1, Supplementary Figure S1)
The motility of the non-aggregating single cells we observe rules out the possibility that these cells are sporulating without aggregating, as in single cell encystation that has been reported for other Dictyostelium species but not so far in D. discoideum[10]
Summary
Every organism has a set of optimal conditions that maximizes its fitness (growth, reproduction and survival). Differentiation on a stochastic basis into different phenotypic states adapted to different environments, known as risk spreading or bet hedging, has been proposed as an adaptation to environmental variation[2,3,4,5,6]. For entering and exiting the dormant state, cells or organisms depend on environmental cues. These cues are not always reliable indicators of the future environment. In such unpredictable environments it pays off for a plant, for instance, to have its seeds germinating stochastically at different time scales to insure that at least some of them will germinate at the time that is beneficial for its growth[7]
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