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Review
. 2015 Nov 20;427(23):3722-33.
doi: 10.1016/j.jmb.2015.08.008. Epub 2015 Aug 15.

The Evolution of Aggregative Multicellularity and Cell-Cell Communication in the Dictyostelia

Qingyou Du  1 , Yoshinori Kawabe  2 , Christina Schilde  3 , Zhi-Hui Chen  4 , Pauline Schaap  5
Affiliations
Review

The Evolution of Aggregative Multicellularity and Cell-Cell Communication in the Dictyostelia

Qingyou Du et al. J Mol Biol. .

Abstract

Aggregative multicellularity, resulting in formation of a spore-bearing fruiting body, evolved at least six times independently amongst both eukaryotes and prokaryotes. Amongst eukaryotes, this form of multicellularity is mainly studied in the social amoeba Dictyostelium discoideum. In this review, we summarise trends in the evolution of cell-type specialisation and behavioural complexity in the four major groups of Dictyostelia. We describe the cell-cell communication systems that control the developmental programme of D. discoideum, highlighting the central role of cAMP in the regulation of cell movement and cell differentiation. Comparative genomic studies showed that the proteins involved in cAMP signalling are deeply conserved across Dictyostelia and their unicellular amoebozoan ancestors. Comparative functional analysis revealed that cAMP signalling in D. discoideum originated from a second messenger role in amoebozoan encystation. We highlight some molecular changes in cAMP signalling genes that were responsible for the novel roles of cAMP in multicellular development.

Keywords: cyclic nucleotide; dual component signalling; encystation; evolution of multicellularity; sporulation.

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Figures

None
Graphical abstract
Fig. 1
Fig. 1
Organisms with aggregative multicellularity. Unicellular eukaryotes mostly have a simple life cycle consisting of a trophozoite feeding stage and a dormant cyst stage. In most eukaryote divisions and in prokaryotes, multicellular forms that aerially lift dormant spores or cysts in fruiting bodies evolved (sorocarps). Starving Myxococcus bacteria aggregate to form fruiting bodies, in which part of the rod-shaped bacteria differentiate into spherical spores. Acrasis amoebae aggregate and start encysting at the base of the structure. Other amoebae crawl to the top, rearrange themselves into chains and then encyst. Guttulinopsis amoebae construct a column surrounded by an elastic sheath. Some amoebae move to the top and differentiate as spores, whilst the remaining amoebae gradually disintegrate. The ciliate Sorogena aggregates by cell adhesion to form a mound encased in a mucous sheath. The sheath contracts to form a stalk that lift up the cells, which then encyst. Fonticula amoebae deposit a cone-shaped matrix around the aggregates. The amoebae then differentiate into spores and are expulsed through the apex. Copromyxa amoebae move towards a few encysted founder cells. Once aggregated, cells crawl on top of existing cysts and then encyst themselves. Dictyostelium aggregates first form migrating slugs. Inside the slug, the cells differentiate into precursors for the spore, stalk, basal disc and upper and lower cup cells. During fruiting formation, the precursor cell types move to their appropriate locations and complete the differentiation process.
Fig. 2
Fig. 2
Cell signalling during Dictyostelium development. (a) The asexual life cycle of D. discoideum. (b) Cell signalling mechanisms. The schematic shows the signals (in red) that control the life cycle transitions and the differentiation of amoebae in spores and somatic cell types. The enzymes that synthesise secreted signal molecules are shown in green text, and proteins and small molecules involved in the intracellular signal transduction pathway are in blue text. Blue arrows and t-crosses denote stimulatory and inhibitory effects, respectively. Double blue arrows signify that no components of the signal transduction pathway are known. All pathways are described in detail in the main text. Abbreviations: PSF: prestarvation factor; MPBD: 4-methyl-5-pentylbenzene-1,3-diol; cAMP: 3′-5′-cyclic adenosine monophosphate; CMF: conditioned medium factor; Tgr: transmembrane, IPT, IG, E-set, repeat protein; DIF-1: differentiation inducing factor 1; c-di-GMP: 3′,5′-cyclic diguanylic acid; NH3: ammonia; SDF-2: spore differentiation factor 2; StlA: Steely A; AcaA: adenylate cyclase A; StlB: Steely B; AcgA: adenylate cyclase G; DmtA: des-methyl-DIF-1 methyltransferase; ChlA: chlorination A; DgcA: diguanylate cyclase A; YakA: DYRK family protein kinase; PufA: pumilio RNA-binding protein; PkaC: cAMP-dependent protein kinase, catalytic subunit; CarA: cAMP receptor 1; GtaC: GATA-binding transcription factor C; DimB: transcription factor DIF-insensitive mutant B; RegA: cAMP phosphodiesterase RegA; AcrA: adenylate cyclase R DhkA: histidine phosphatase A; DhkB: histidine kinase B; DhkC: histidine kinase C; DokA: osmosensing histidine phosphatase.
Fig. 3
Fig. 3
Hypothetical scenario for the evolution of developmental cAMP signalling in Dictyostelia. The cAMP signalling mechanisms that coordinate Dictyostelium development likely evolved from a core function of cAMP as intermediate for stress-induced encystation in the unicellular ancestor. In this role, stress acts on sensor histidine phosphatases to inhibit the cAMP phosphodiesterase RegA, allowing cAMP levels, produced by AcgA or AcrA, to increase and activate PKA, which subsequently induces encystation. The roles of secreted cAMP in induction of spore formation and in coordination of fruiting body morphogenesis evolved later, with the chemoattractant role of cAMP during aggregation only emerging in the last common ancestor (LCA) to group 4.
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References

    1. He D., Fiz-Palacios O., Fu C.J., Fehling J., Tsai C.C., Baldauf S.L. An alternative root for the eukaryote tree of life. Curr. Biol. 2014;24:465–470. - PubMed
    1. Pawlowski J., Audic S., Adl S., Bass D., Belbahri L., Berney C., Bowser S.S., Cepicka I., Decelle J., Dunthorn M., Fiore-Donno A.M., Gile G.H., Holzmann M., Jahn R., Jirku M., Keeling P.J., Kostka M., Kudryavtsev A., Lara E., Lukes J., Mann D.G., Mitchell E.A., Nitsche F., Romeralo M., Saunders G.W., Simpson A.G., Smirnov A.V., Spouge J.L., Stern R.F., Stoeck T., Zimmermann J., Schindel D., de Vargas C. CBOL protist working group: Barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol. 2012;10:e1001419. - PMC - PubMed
    1. Velicer G.J., Vos M. Sociobiology of the myxobacteria. Annu. Rev. Microbiol. 2009;63:599–623. - PubMed
    1. Brown M.W., Silberman J.D., Spiegel F.W. A contemporary evaluation of the acrasids (Acrasidae, Heterolobosea, Excavata) Eur. J. Protistol. 2012;48:103–123. - PubMed
    1. Brown M.W., Spiegel F.W., Silberman J.D. Phylogeny of the “forgotten” cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol. Biol. Evol. 2009;26:2699–2709. - PubMed

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