Mind the gap: a comparative study of migratory behavior in social amoebae

Social amoebae aggregate to form a multicellular slug that migrates some distance. Most species produce a stalk during migration, but some do not. We show that Dictyostelium giganteum, a species that produces stalk during migration, is able to traverse small gaps and utilize bacterial resources following gap traversal by shedding live cells. In contrast, we found that Dictyostelium discoideum, a species that does not produce stalk during migration, can traverse gaps only when in the presence of other species’ stalks or other thin filaments. These findings suggest that production of stalk during migration allows traversal of gaps that commonly occurs in soil and leaf litter. Considering the functional consequences of a stalked migration may be important for explaining the evolutionary maintenance or loss of a stalked migration

The Rate and Effects of Spontaneous Mutation on Fitness Traits in the Social Amoeba, Dictyostelium discoideum

We performed a mutation accumulation (MA) experiment in the social amoeba Dictyostelium discoideum to estimate the rate and distribution of effects of spontaneous mutations affecting eight putative fitness traits. We found that the per-generation mutation rate for most fitness components is 0.0019 mutations per haploid genome per generation or larger. This rate is an order of magnitude higher than estimates for fitness components in the unicellular eukaryote Saccharomyces cerevisiae, even though the base-pair substitution rate is two orders of magnitude lower. The high rate of fitness-altering mutations observed in this species may be partially explained by a large mutational target relative to S. cerevisiae. Fitness-altering mutations also may occur primarily at simple sequence repeats, which are common throughout the genome, including in coding regions, and may represent a target that is particularly likely to give fitness effects upon mutation. The majority of mutations had deleterious effects on fitness, but there was evidence for a substantial fraction, up to 40%, being beneficial for some of the putative fitness traits. Competitive ability within the multicellular slug appears to be under weak directional selection, perhaps reflecting the fact that slugs are sometimes, but not often, comprised of multiple clones in nature. Evidence for pleiotropy among fitness components across MA lines was absent, suggesting that mutations tend to act on single fitness components

The multicellularity genes of dictyostelid social amoebas

The evolution of multicellularity enabled specialization of cells, but required novel signalling mechanisms for regulating cell differentiation. Early multicellular organisms are mostly extinct and the origins of these mechanisms are unknown. Here using comparative genome and transcriptome analysis across eight uni- and multicellular amoebozoan genomes, we find that 80% of proteins essential for the development of multicellular Dictyostelia are already present in their unicellular relatives. This set is enriched in cytosolic and nuclear proteins, and protein kinases. The remaining 20%, unique to Dictyostelia, mostly consists of extracellularly exposed and secreted proteins, with roles in sensing and recognition, while several genes for synthesis of signals that induce cell-type specialization were acquired by lateral gene transfer. Across Dictyostelia, changes in gene expression correspond more strongly with phenotypic innovation than changes in protein functional domains. We conclude that the transition to multicellularity required novel signals and sensors rather than novel signal processing mechanisms

An invitation to die: initiators of sociality in a social amoeba become selfish spores

Greater size and strength are common attributes of contest winners. Even in social insects with high cooperation, the right to reproduce falls to the well-fed queens rather than to poorly fed workers. In Dictyostelium discoideum, formerly solitary amoebae aggregate when faced with starvation, and some cells die to form a stalk which others ride up to reach a better location to sporulate. The first cells to starve have lower energy reserves than those that starve later, and previous studies have shown that the better-fed cells in a mix tend to form disproportionately more reproductive spores. Therefore, one might expect that the first cells to starve and initiate the social stage should act altruistically and form disproportionately more of the sterile stalk, thereby enticing other better-fed cells into joining the aggregate. This would resemble caste determination in social insects, where altruistic workers are typically fed less than reproductive queens. However, we show that the opposite result holds: the first cells to starve become reproductive spores, presumably by gearing up for competition and outcompeting late starvers to become prespore first. These findings pose the interesting question of why others would join selfish organizers

Two-Dimensionality of Yeast Colony Expansion Accompanied by Pattern Formation

<div><p>Yeasts can form multicellular patterns as they expand on agar plates, a phenotype that requires a functional copy of the <i>FLO11</i> gene. Although the biochemical and molecular requirements for such patterns have been examined, the mechanisms underlying their formation are not entirely clear. Here we develop quantitative methods to accurately characterize the size, shape, and surface patterns of yeast colonies for various combinations of agar and sugar concentrations. We combine these measurements with mathematical and physical models and find that <i>FLO11</i> gene constrains cells to grow near the agar surface, causing the formation of larger and more irregular colonies that undergo hierarchical wrinkling. Head-to-head competition assays on agar plates indicate that two-dimensional constraint on the expansion of <i>FLO11 wild type</i> (<i>FLO11</i>) cells confers a fitness advantage over <i>FLO11 knockout</i> (<i>flo11</i>Δ) cells on the agar surface.</p></div

Colony size and irregularity for various glucose and agar concentrations.

<p><i>(A, B)</i> Images of <i>FLO11 (A)</i> and <i>flo11Δ (B)</i> on YPD plates containing different glucose (0.5%, 1.0%, 2.0%) and agar (1.5%, 3.0%, 6.0%) concentrations around day 20. <i>(C, D)</i> The expansion of colony area <i>(C)</i> and the irregularity <i>(D)</i> of <i>FLO11</i> (red curves) and <i>flo11Δ</i> (green curves) colonies over the 60-day time course. <i>FLO11</i> colonies (red curves) demonstrated higher maximum colony size <i>(C)</i> with higher irregularity <i>(D)</i> at the colony rim than the <i>flo11Δ</i> colonies (green curves) in all conditions tested. The maximum colony size <i>(C)</i> of both <i>FLO11</i> (red curves) and <i>flo11Δ</i> (green curves) colonies increased with glucose and inversely depended on agar concentrations. The irregularity of <i>FLO11 (D)</i> (red curves) inversely depended on both the agar and the glucose concentrations, compared to the minimal irregularity of <i>flo11Δ (D)</i> (green curves) colonies throughout the time course at all conditions tested. Thinner curves represent different replicates while thicker curves represent their average up until all the replicates were present.</p

Mathematical model of colony expansion.

<p><i>(A–C)</i> A snapshot of the colonies at the end of simulation. Although these simulations are started with circular colonies, over time petals appear. The color scale represents cell density (arbitrary units). <i>(D–F)</i> The maximum colony area is higher upon higher initial glucose concentration, in agreement with the experimental results in <a href="http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003979#pcbi-1003979-g001" target="_blank">Fig. 1</a>. The dimensionless “colony area ratio” was the ratio of colony area to the area of simulation box, and glucose concentration corresponded to the initial value of glucose in the simulation, and was chosen as a constant over space. Time is a rescaled variable measured in arbitrary units. <i>(G–I)</i> Simulated colony irregularity (P2A) plotted as a function of time. Similar to experiments (<a href="http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003979#pcbi-1003979-g001" target="_blank">Fig. 1</a>), in our model P2A is initially at a basal level and then increases abruptly to a large value. This increase in P2A corresponds to petal formation and occurs as a result of competition over glucose among cells that make up the colony rim. Interestingly, the maximum value of P2A decreases with increasing glucose levels. This result is likely due to decreased intercellular competition over nutrients in the early stages of expansion and is compatible with experiments in <a href="http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003979#pcbi-1003979-g001" target="_blank">Fig. 1</a>, where colonies exhibit less structure as glucose levels increase.</p