The Amphimedon queenslandica genome and the evolution of animal complexity

Abstract

Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse 'toolkit' of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.

Figure 1

a, Amphimedon queenslandica adult. Scale bar, 5 cm. b, Embryos in a brood chamber. Scale bar, 1 mm. c, Larva. Scale bar, 100 µm. d, Animal phylogeny based on whole-genome data. This unrooted tree is inferred from 229 concatenated nuclear protein-coding genes with 44,616 amino acids using Bayesian inference. All clades are supported with a posterior probability of 1. Coloured boxes mark the nodes for which origins of genes are inferred in Figs 3 and 4. The same topology is supported by the nuclear gene data sets generated by alternative methods as well as by other inference methods (Supplementary Note 7). The metazoan stem leading to the animal radiation is shown in bold. Contrary to the current consensus of eukaryotic relationships, Amoebozoa are not a sister-group to Opisthokonta in this tree (Supplementary Note 7).

Figure 2. Origins of vertebrate/bilaterian pathways

Reference pathways from human and other vertebrates are depicted here for comparative purposes. Gene products are coloured by their node of origin as per Fig. 1. White text denotes known oncogenes or tumour suppressor genes. Genes with eumetazoan origin are found in either Nematostella or Trichoplax or both. a, Cell cycle; b, cell growth; c, apoptosis. Dashed lines indicate cases where proteins could not be affiliated to a subtype (see Supplementary Note 8.3).

Figure 3. Origins of complexes and pathways of bilaterian cell types

Reference cellular structures from human and other vertebrates are depicted here for comparative purposes. Gene products are coloured in by their node of origin as per Fig. 1. White text denotes known oncogenes or tumour suppressor genes. Genes with eumetazoan origin are found in either Nematostella or Trichoplax or both. a, Cell adhesion and polarity in epithelia. The asterisk indicates that collagen IV genes have not been found in the Amphimedon genome but have been reported as present in the homoscleromorph sponge Pseudocorticium jarrei. b, Synaptic and signalling elements in neurons.

Figure 4. Molecular functions enriched in various complexity groups

Molecular function categories that show significant enrichment (1×10⁻¹⁰) in Fisher’s exact tests were selected (Supplementary Note 11). Significance of enrichments (grey background) and depletions (white background) for the three ‘metazoan complexity groups’ (non-bilaterian metazoans; invertebrate bilaterians; vertebrates) are indicated in the columns to the left of the heatmap. The heatmap shows normalized gene counts of PANTHER molecular function categories for the species in the analysis. Aqu, Amphimedon queenslandica; Ath, Arabidopsis thaliana; Cel, Caenorhabditis elegans; Ddi, Dictyostelium discoideum; Dme, Drosophila melanogaster; Hma, Hydra magnipapillata; Hsa, Homo sapiens; Mbr, Monosiga brevicollis; Ncr, Neurospora crassa; Nve, Nematostella vectensis; Pte, Paramecium tetraurelia; Spu, Strongylocentrotus purpuratus; Tad, Trichoplax adhaerens.