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Insights into bilaterian evolution from three spiralian genomes.

ABSTRACT: Current genomic perspectives on animal diversity neglect two prominent phyla, the molluscs and annelids, that together account for nearly one-third of known marine species and are important both ecologically and as experimental systems in classical embryology. Here we describe the draft genomes of the owl limpet (Lottia gigantea), a marine polychaete (Capitella teleta) and a freshwater leech (Helobdella robusta), and compare them with other animal genomes to investigate the origin and diversification of bilaterians from a genomic perspective. We find that the genome organization, gene structure and functional content of these species are more similar to those of some invertebrate deuterostome genomes (for example, amphioxus and sea urchin) than those of other protostomes that have been sequenced to date (flies, nematodes and flatworms). The conservation of these genomic features enables us to expand the inventory of genes present in the last common bilaterian ancestor, establish the tripartite diversification of bilaterians using multiple genomic characteristics and identify ancient conserved long- and short-range genetic linkages across metazoans. Superimposed on this broadly conserved pan-bilaterian background we find examples of lineage-specific genome evolution, including varying rates of rearrangement, intron gain and loss, expansions and contractions of gene families, and the evolution of clade-specific genes that produce the unique content of each genome.

SUBMITTER: Simakov O

PROVIDER: S-EPMC4085046 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Insights into bilaterian evolution from three spiralian genomes.

Simakov Oleg O Marletaz Ferdinand F Cho Sung-Jin SJ Edsinger-Gonzales Eric E Havlak Paul P Hellsten Uffe U Kuo Dian-Han DH Larsson Tomas T Lv Jie J Arendt Detlev D Savage Robert R Osoegawa Kazutoyo K de Jong Pieter P Grimwood Jane J Chapman Jarrod A JA Shapiro Harris H Aerts Andrea A Otillar Robert P RP Terry Astrid Y AY Boore Jeffrey L JL Grigoriev Igor V IV Lindberg David R DR Seaver Elaine C EC Weisblat David A DA Putnam Nicholas H NH Rokhsar Daniel S DS

Nature 20121219 7433

Current genomic perspectives on animal diversity neglect two prominent phyla, the molluscs and annelids, that together account for nearly one-third of known marine species and are important both ecologically and as experimental systems in classical embryology. Here we describe the draft genomes of the owl limpet (Lottia gigantea), a marine polychaete (Capitella teleta) and a freshwater leech (Helobdella robusta), and compare them with other animal genomes to investigate the origin and diversific ...[more]

PMID: 23254933

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Project description:BackgroundObtaining phylogenomic data for enigmatic taxa is essential to achieve a better understanding of animal evolution. Dicyemids have long fascinated biologists because of their highly simplified body organization, but their life-cycles remain poorly known. Based on the discovery of the dicyemid DoxC gene, which encodes a spiralian peptide, it has been proposed that dicyemids are members of the Spiralia. Other studies have suggested that dicyemids may have closer affinities to mollusks and annelids. However, the phylogenetic position of dicyemids has remained a matter of debate, leading to an ambiguous picture of spiralian evolution.ResultsIn the present study, newly sequenced transcriptomic data from Dicyema japonicum were complemented with published transcriptomic data or predicted gene models from 29 spiralian, ecdysozoan, and deuterostome species, generating a dataset (Dataset 1) for phylogenomic analyses, which contains 348 orthologs and 58,124 amino acids. In addition to this dataset, to eliminate systematic errors, two additional sub-datasets were created by removing compositionally heterogeneous or rapidly evolving sites and orthologs from Dataset 1, which may cause compositional heterogeneity and long-branch attraction artifacts. Maximum likelihood and Bayesian inference analyses both placed Dicyema japonicum (Dicyemida) in a clade with Intoshia linei (Orthonectida) with strong statistical support. Furthermore, maximum likelihood analyses placed the Dicyemida + Orthonectida clade within the Gastrotricha, while in Bayesian inference analyses, this clade is sister group to the clade of Gastrotricha + Platyhelminthes.ConclusionsWhichever the case, in all analyses, Dicyemida, Orthonectida, Gastrotricha, and Platyhelminthes constitute a monophyletic group that is a sister group to the clade of Mollusca + Annelida. Based on present phylogenomic analyses, dicyemids display close affinity to orthonectids, and they may share a common ancestor with gastrotrichs and platyhelminths, rather than with mollusks and annelids. Regarding spiralian phylogeny, the Gnathifera forms the sister group to the Rouphozoa and Lophotrochozoa, as has been suggested by previous studies; thus our analysis supports the traditional acoeloid-planuloid hypothesis of a nearly microscopic, non-coelomate common ancestor of spiralians.

Project description:A general trend observed in animal skeletomes-the proteins occluded in animal skeletons-is the copresence of taxonomically widespread and lineage-specific proteins that actively regulate the biomineralization process. Among cnidarians, the skeletomes of scleractinian corals have been shown to follow this trend. However, distributions and phylogenetic analyses of biomineralization-related genes are often based on only a few species, with other anthozoan calcifiers such as octocorals (soft corals), not being fully considered. We de novo assembled the transcriptomes of four soft-coral species characterized by different calcification strategies (aragonite skeleton vs. calcitic sclerites) and data-mined published nonbilaterian transcriptome resources to construct a taxonomically comprehensive sequence database to map the distribution of scleractinian and octocoral skeletome components. Cnidaria shared no skeletome proteins with Placozoa or Ctenophora, but did share some skeletome proteins with Porifera, such as galaxin-related proteins. Within Scleractinia and Octocorallia, we expanded the distribution for several taxonomically restricted genes such as secreted acidic proteins, scleritin, and carbonic anhydrases, and propose an early, single biomineralization-recruitment event for galaxin sensu stricto. Additionally, we show that the enrichment of acidic residues within skeletogenic proteins did not occur at the Corallimorpharia-Scleractinia transition, but appears to be associated with protein secretion into the organic matrix. Finally, the distribution of octocoral calcification-related proteins appears independent of skeleton mineralogy (i.e., aragonite/calcite) with no differences in the proportion of shared skeletogenic proteins between scleractinians and aragonitic or calcitic octocorals. This points to skeletome homogeneity within but not between groups of calcifying cnidarians, although some proteins such as galaxins and SCRiP-3a could represent instances of commonality.

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Insights into bilaterian evolution from three spiralian genomes.

Publications

Insights into bilaterian evolution from three spiralian genomes.

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