Evolution of Multicellular Complexity in The Dictyostelid Social Amoebas

Abstract

Multicellularity evolved repeatedly in the history of life, but how it unfolded varies greatly between different lineages. Dictyostelid social amoebas offer a good system to study the evolution of multicellular complexity, with a well-resolved phylogeny and molecular genetic tools being available. We compare the life cycles of the Dictyostelids with closely related amoebozoans to show that complex life cycles were already present in the unicellular common ancestor of Dictyostelids. We propose frost resistance as an early driver of multicellular evolution in Dictyostelids and show that the cell signalling pathways for differentiating spore and stalk cells evolved from that for encystation. The stalk cell differentiation program was further modified, possibly through gene duplication, to evolve a new cell type, cup cells, in Group 4 Dictyostelids. Studies in various multicellular organisms, including Dictyostelids, volvocine algae, and metazoans, suggest as a common principle in the evolution of multicellular complexity that unicellular regulatory programs for adapting to environmental change serve as "proto-cell types" for subsequent evolution of multicellular organisms. Later, new cell types could further evolve by duplicating and diversifying the "proto-cell type" gene regulatory networks.

Keywords: amoebozoa; cAMP signalling; cell type evolution; dictyostelia; encystation; evolution of multicellularity.

Figure 1

Life cycles of Amoebozoan groups related to the Dictyostelids. (A). The Dictyostelids show four different cycles, the unicellular vegetative and encystation cycles and the multicellular sexual and sorocarpic cycles. The depiction of the sorocarpic multicellular cycle shows generalised differences between Dictyostelids in Groups 1–3 and those in Group 4. Different cell types in the fruiting body are shown in different colours. Cup cells and basal disc cells are found only in Group 4, while encystation is lost in this group. (B). The Myxogastrids show three major life cycles, vegetative, plasmodial (or sexual), and encystation, as depicted here. In addition, not shown here, the plasmodium can turn into a dormant dehydrated structure, called sclerotium, in harsh environmental conditions, and can also be produced with haploid cells (apogametic cycle). Redrawn after Figure 5 in [35]. (C). In many species of Archaemoeba, multiple cellular phenotypes, such as amoeba, multinucleate amoeba, cyst, and flagellate are known to exist, but there is not much information about how they transition from one to another. Redrawn after Figure 1 in [36].

Figure 2

Time tree of Amoebozoa. A. Simplified tree of Amoebozoa with a few related groups of eukaryotes, representing the relationships of major groups. The positions of the 4 major groups of Dictyostelia are indicated. Divergence time is shown in 100 million years. Blue bars on the nodes represent Bayesian 95% Highest Posterior Density (HPD) intervals. Major global glaciation periods are shown above the tree. Redrawn from Figure 5 in [26].

Figure 3

Dictyostelid signalling pathways evolved from an amoebozoan stress response. (A). In solitary amoebas, starvation or drought stress increases intracellular cAMP levels to activate (PKA), which induces the transition from growing trophozoite into walled dormant cyst. The cAMP phosphodiesterase, RegA, inhibits this process by hydrolysing cAMP; it bears a conserved response regulator domain that is the target for phosphorylation/dephosphorylation by sensor histidine kinases/phosphatase (SHK/Ps) that, respectively, activate/inactivate the hydrolytic activity. The signal module of SHK/Ps, RegA, PKA, and AcrA is conserved throughout Amoebozoa. (B,C) In the multicellular Dictyostelids, this stress pathway came under control of signals exchanged between the cells that regulate the differentiation of walled spores and stalk cells. See main text for details. Other abbreviations: AcrA, AcgA, AcaA: adenylate cyclases R, G, and A; PKA: cAMP-dependent protein kinase; cAR: cell surface cAMP receptor; DhkC: sensor histidine kinase C; DhkA: sensor histidine phosphatase A; TagC: tight aggregate C—a protease; AcbA: acetyl-coA-binding protein A, the precursor of SDF2: spore differentiation factor 2—a peptide; DIF-1: differentiation factor 1—a chlorinated polyketide; c-di-GMP: 3’,5’-cyclic diguanylic acid.