Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication

Abstract

Dictyostelium discoideum (DD), an extensively studied model organism for cell and developmental biology, belongs to the most derived group 4 of social amoebas, a clade of altruistic multicellular organisms. To understand genome evolution over long time periods and the genetic basis of social evolution, we sequenced the genomes of Dictyostelium fasciculatum (DF ) and Polysphondylium pallidum (PP), which represent the early diverging groups 1 and 2, respectively. In contrast to DD, PP and DF have conventional telomere organization and strongly reduced numbers of transposable elements. The number of proteincoding genes is similar between species, but only half of them comprise an identifiable set of orthologous genes. In general, genes involved in primary metabolism, cytoskeletal functions and signal transduction are conserved, while genes involved in secondary metabolism, export, and signal perception underwent large differential gene family expansions. This most likely signifies involvement of the conserved set in core cell and developmental mechanisms, and of the diverged set in niche-and species-specific adaptations for defense and food, mate, and kin selection. Phylogenetic dating using a concatenated data set and extensive loss of synteny indicate that DF, PP, and DD split from their last common ancestor at least 0.6 billion years ago.[Supplemental material is available for this article.]The central and most fascinating problem in biology is how natural selection has acted on random changes in the genomes of individuals to generate the immense range and complexity of extinct and extant living forms. However, understanding the relationship between genotypic and phenotypic change on a genomewide scale is complicated by the large number of loci involved and the range of phenotypic change. Comparative genomics is the tool of choice to define common gene sets and the first occurrence of genetic changes that may have caused phenotypic innovation. Genetic manipulation of altered genes can then reveal whether the genomic change was causal to the phenotypic alteration.The social amoeba Dictyostelium discoideum (DD) is a widely used model system for studying a range of problems in cell and developmental biology and more recently the evolution of social behavior and multicellularity.

An ancestral bacterial division system is widespread in eukaryotic mitochondria

“…Here, D. discoideum, Dictyostelium citrinum, Dictyostelium intermedium, and Dictyostelium firmibasis have retained only FtsZ whereas their sister taxon D. purpureum and the more basal taxa P. pallidum, Polysphondylium violaceum, and A. subglobosum have additionally maintained all three Min proteins. Meanwhile, the yet more distantly related Dictyostelium fasciculatum (72,73) seems to have independently lost the Min proteins and, like D. discoideum, only possesses FtsZ. This overall pattern raises the question of why Min proteins were retained in some taxa, yet lost in others.…”

Multicellularity arose several times in the evolution of eukaryotes (Response to DOI 10.1002/bies.201100187)

“…There have been numerous gene duplications and subfunctionalization of a-catenin within animals, and especially vertebrates [20,22]. Vinculins are present in the unicellular relatives of animals, including Capsaspora [23] and Dictyostelium [6,11], but are not found in most eukaryotes [23]. b-Catenin, on the other hand, has experienced many gene duplications, especially within animals [20,21], and homologs of b-catenin are widely distributed across eukaryotes.…”

“…D. discoideum has homologs of both a-catenin and b-catenin called Dd a-catenin and Aardvark, respectively [11,18], as well as an additional member of the vinculin family [6,9]. Dd a-catenin localizes to the cell surface during the multicellular phase of the life cycle (but crucially not when Dictyostelium is unicellular [11]) and shares biochemical properties with metazoan a-catenin, but not vinculin [11].…”

“…The dictyostelids are alternatively referred to as cellular slime molds or social amoebae. There are three described genera of dictyostelids, however molecular analyses demonstrate that these intermingle, and the actual diversity within this ancient clade is much greater [4,6]. Dictyostelid amoebae spend much of their life cycle foraging in soils and leaf litter for bacteria as single celled amoebae.…”

Evolution of self-organisation in Dictyostelia by adaptation of a non-selective phosphodiesterase and a matrix component for regulated cAMP degradation

“…The PCR program consisted of 35 cycles, with 30 seconds at 95°C, 50°C and 68°C each, and yielded products of about 300 bp from Pvio, Drhi, Aana, Daus and Dfas gDNAs. Full length D. purpureum (Dpur), Dfas, Ppal, Acytostelium subglobosum (Asub) and D. lacteum (Dlac) PdsA genes are recently available from ongoing genome sequencing projects (Heidel et al, 2011;Sucgang et al, 2011) (http://acytodb.biol.tsukuba.ac.jp/cgi-bin/index.cgi?.orgas) (P.S. and G. Gloeckner, unpublished results).…”