Demosponge EST Sequencing Reveals a Complex Genetic Toolkit of the Simplest Metazoans

Abstract

Sponges (Porifera) are among the simplest living and the earliest branching metazoans. They hold a pivotal role for studying genome evolution of the entire metazoan branch, both as an outgroup to Eumetazoa and as the closest branching phylum to the common ancestor of all multicellular animals (Urmetazoa). In order to assess the transcription inventory of sponges, we sequenced expressed sequence tag libraries of two demosponge species, Suberites domuncula and Lubomirskia baicalensis, and systematically analyzed the assembled sponge transcripts against their homologs from complete proteomes of six well-characterized metazoans—Nematostella vectensis, Caenorhabditis elegans, Drosophila melanogaster, Strongylocentrotus purpuratus, Ciona intestinalis, and Homo sapiens. We show that even the earliest metazoan species already have strikingly complex genomes in terms of gene content and functional repertoire and that the rich gene repertoire existed even before the emergence of true tissues, therefore further emphasizing the importance of gene loss and spatio-temporal changes in regulation of gene expression in shaping the metazoan genomes. Our findings further indicate that sponge and human genes generally show similarity levels higher than expected from their respective positions in metazoan phylogeny, providing direct evidence for slow rate of evolution in both “basal” and “apical” metazoan genome lineages. We propose that the ancestor of all metazoans had already had an unusually complex genome, thereby shifting the origins of genome complexity from Urbilateria to Urmetazoa.

Characterization of Nme6-like gene/protein from marine sponge Suberites domuncula

“…They have no true tissues and organs and lead a sessile lifestyle. Due to the fact that they have changed little during evolution, they probably provide the best insight into the metazoan ancestors' genomic features (Cetkovic et al 2004;Perina et al 2006;Cetkovic et al 2007;Philippe et al 2009;Harcet et al 2010;Srivastava et al 2010). Real number of the Nme proteins in sponge Suberites domuncula is possibly higher than we previously reported because EST database used in S. domuncula Nme study (Harcet et al 2005) contained at most 4500 non-redundant cDNA sequences, which is certainly far less than the total number of genes in the S. domuncula genome.…”

Virtual Genomes in Flux: An Interplay of Neutrality and Adaptability Explains Genome Expansion and Streamlining

“…Rapid genomic and intronic expansion was most likely the driving force behind the radiation of the eumetazoan lineage (Putnam et al 2007; Harcet et al 2010; Srivastava et al 2010), playing out at an intermediate evolutionary depth. In multiple plant species, whole genome duplications have been associated with drastic changes in the environment (Blanc and Wolfe 2004; Van de Peer et al 2009), potentially enabling these species to survive.…”

Characterization of Bruton’s Tyrosine Kinase Gene and Protein from Marine Sponge Suberites domuncula

“…Systematic analysis of the sponge gene repertoire showed that the genomic complexity was already present at the very beginning of metazoan evolution, before the appearance of tissue or any other complex morphological feature found in extant animals. 10 Previous analyses of phylogenetically conserved genes/proteins in sponges identified a number of very sophisticated multifunctional enzymes whose functions are usually associated with human diseases. 3,11,12 Btk-like 700-aa-long protein from the marine sponge Suberites domuncula (Demospongia) was described previously.…”