The social amoebae are exceptional in their ability to alternate between unicellular and multicellular forms. Here we describe the genome of the best-studied member of this group, Dictyostelium discoideum. The gene-dense chromosomes encode ~12,500 predicted proteins, a high proportion of which have long repetitive amino acid tracts. There are many genes for polyketide synthases and ABC transporters, suggesting an extensive secondary metabolism for producing and exporting small molecules. The genome is rich in complex repeats, one class of which is clustered and may serve as centromeres. Partial copies of the extrachromosomal rDNA element are found at the ends of each chromosome, suggesting a novel telomere structure and the use of a common mechanism to maintain both the rDNA and chromosomal termini. A proteome-based phylogeny shows that the amoebozoa diverged from the animal/fungal lineage after the plant/animal split, but Dictyostelium appears to have retained more of the diversity of the ancestral genome than either of these two groups.The amoebozoa are a richly diverse group of organisms whose genomes remain largely unexplored. The soil-dwelling social amoeba Dictyostelium discoideum has been actively studied for the past fifty years and has contributed greatly to our understanding of cellular motility, signalling and interaction 1 . For example, studies in Dictyostelium provided the first descriptions of a eukaryotic cell chemo-attractant and a cell-cell adhesion protein 2, 3 .Dictyostelium amoebae inhabit forest soil consuming bacteria and yeast, which they track by chemotaxis. Starvation, however, prompts the solitary cells to aggregate and to develop as a true multicellular organism, producing a fruiting body comprised of a cellular, cellulosic stalk supporting a bolus of spores. Thus, Dictyostelium has evolved mechanisms that direct the differentiation of a homogeneous population of cells into distinct cell types, regulate the proportions between tissues and orchestrate the construction of an effective structure for the dispersal of spores 4 . Many of the genes necessary for these processes in Dictyostelium were Eichinger et al. Page 2 Nature. Author manuscript; available in PMC 2006 January 27. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript also inherited by metazoa and fashioned through evolution for use within many different modes of development.The amoebozoa are also noteworthy as representing one of the earliest branches from the last common ancestor of all eukaryotes. Each of the surviving branches of the crown group of eukaryotes provides an example of the ways in which the ancestral genome has been sculpted and adapted by lineage-specific gene duplication, divergence and deletion. Comparison between representatives of these branches promises to shed light not only on the nature and content of the ancestral eukaryotic genome, but on the diversity of ways in which its components have been adapted to meet the needs of complex organisms. The genome of Dictyosteliu...

Transcriptional profiling of Dictyostelium development reveals significant conservation of transcriptional profiles between evolutionarily divergent species.

Summary Self- and kin-discrimination are observed in most kingdoms of life and are mediated by highly polymorphic plasma membrane proteins [1-7]. Sequence polymorphism, which is essential for effective recognition, is maintained by balancing selection [8-10]. Dictyostelium discoideum are social amoebae that propagate as unicellular organisms, but aggregate upon starvation and from fruiting bodies with viable spores and dead stalk cells. Aggregative development exposes Dictyostelium to the perils of chimerism, including cheating, which raises questions about how the victims survive in nature and how social cooperation persists [11-15]. Dictyostelids can minimize the cost of chimerism by preferential cooperation with kin [16-18], but the mechanisms of kin-discrimination are largely unknown. Dictyostelium lag-genes encode transmembrane proteins with multiple immunoglobulin (Ig) repeats that participate in cell-adhesion and signaling [19-25]. Here we describe their role in kin-discrimination. We show that lagB1 and lagC1 are highly polymorphic in natural populations and that their sequence dissimilarity correlates well with wild-strain segregation. Deleting lagB1 and lagC1 results in strain segregation in chimerae with wild-type cells, whereas elimination of the nearly invariant homolog lagD1 has no such consequences. These findings reveal an early evolutionary origin of kin-discrimination and provide insight into the mechanism of social recognition and immunity.

Cooperation is central to many major transitions in evolution, including the emergence of eukaryotic cells, multicellularity and eusociality. Cooperation can be destroyed by the spread of cheater mutants that do not cooperate but gain the benefits of cooperation from others. However, cooperation can be preserved if cheaters are facultative, cheating others but cooperating among themselves. Several cheater mutants have been studied before, but no study has attempted a genome-scale investigation of the genetic opportunities for cheating. Here we describe such a screen in a social amoeba and show that cheating is multifaceted by revealing cheater mutations in well over 100 genes of diverse types. Many of these mutants cheat facultatively, producing more than their fair share of spores in chimaeras, but cooperating normally when clonal. These findings indicate that phenotypically stable cooperative systems may nevertheless harbour genetic conflicts. The opportunities for evolutionary moves and countermoves in such conflicts may select for the involvement of multiple pathways and numerous genes.

BackgroundThe social amoebae (Dictyostelia) are a diverse group of Amoebozoa that achieve multicellularity by aggregation and undergo morphogenesis into fruiting bodies with terminally differentiated spores and stalk cells. There are four groups of dictyostelids, with the most derived being a group that contains the model species Dictyostelium discoideum.ResultsWe have produced a draft genome sequence of another group dictyostelid, Dictyostelium purpureum, and compare it to the D. discoideum genome. The assembly (8.41 × coverage) comprises 799 scaffolds totaling 33.0 Mb, comparable to the D. discoideum genome size. Sequence comparisons suggest that these two dictyostelids shared a common ancestor approximately 400 million years ago. In spite of this divergence, most orthologs reside in small clusters of conserved synteny. Comparative analyses revealed a core set of orthologous genes that illuminate dictyostelid physiology, as well as differences in gene family content. Interesting patterns of gene conservation and divergence are also evident, suggesting function differences; some protein families, such as the histidine kinases, have undergone little functional change, whereas others, such as the polyketide synthases, have undergone extensive diversification. The abundant amino acid homopolymers encoded in both genomes are generally not found in homologous positions within proteins, so they are unlikely to derive from ancestral DNA triplet repeats. Genes involved in the social stage evolved more rapidly than others, consistent with either relaxed selection or accelerated evolution due to social conflict.ConclusionsThe findings from this new genome sequence and comparative analysis shed light on the biology and evolution of the Dictyostelia.