Complete mitochondrial genomes of four deep-sea echinoids: conserved mitogenome organization and new insights into the phylogeny and evolution of Echinoidea

Abstract

Echinoids are an important component in benthic marine environments, which occur at all depths from the shallow-water hard substrates to abyssal depths. To date, the phylogeny of the sea urchins and the macro-evolutionary processes of deep-sea and shallow water groups have not yet been fully resolved. In the present study, we sequenced the complete mitochondrial genomes (mitogenomes) of four deep-sea sea urchins (Echinoidea), which were the first representatives of the orders Aspidodiadematoida, Pedinoida and Echinothurioida, respectively. The gene content and arrangement were highly conserved in echinoid mitogenomes. The tRNA-Ser ^AGY with DHU arm was detected in the newly sequenced echinoid mitogenomes, representing an ancestral structure of tRNA-Ser ^AGY. No difference was found between deep-sea and shallow water groups in terms of base composition and codon usage. The phylogenetic analysis showed that all the orders except Spatangoida were monophyletic. The basal position of Cidaroida was supported. The closest relationship of Scutelloida and Echinolampadoida was confirmed. Our phylogenetic analysis shed new light on the position of Arbacioida, which supported that Arbacioida was most related with the irregular sea urchins instead of Stomopneustoida. The position Aspidodiadematoida (((Aspidodiadematoida + Pedinoida) + Echinothurioida) + Diadematoida) revealed by mitogenomic data discredited the hypothesis based on morphological evidences. The macro-evolutionary pattern revealed no simple onshore-offshore or an opposite hypothesis. But the basal position of the deep-sea lineages indicated the important role of deep sea in generating the current diversity of the class Echinoidea.

Keywords: Deep-sea; Echinoidea; Evolution; Mitochondrial genome; Phylogenetic relationship.

Figure 1. Recent hypotheses of relationships at orders of Echinoidea based on molecular and morphological data.

The studies summarized here reached different conclusions.

Figure 2. The organization of the mitochondrial genome of the four newly determined mitogenomes.

The full names of protein-coding genes and rRNA genes are listed under abbreviations. One uppercase letter amino acid abbreviations are used to label the corresponding tRNA genes. The position of control region (CR) is marked in green, and their stem-loop structures are shown in left. The poly-G stretches are indicated in blue.

Figure 3. A possible evolutionary pathway of tRNA-Ser^AGY gene and secondary structure changes (loss and acquisition of the DHU arms) among mitochondrial genomes of the echinoids.

Figure 4. (A–D) Nucleotide composition and codon usage of of Echinoidea mitogenomes.

Figure 5. Saturation tests and phylogenetic trees inferred from ML and BI methods based the 12 concatenated mitochondrial genes (except atp8 gene).

The bootstrap probability (the first number) and the Bayesian posterior probability (the second number) were shown at each node. The black dots mean 100/1.00. The four echinoid species newly sequenced in the present study have been used bold taxa.

Figure 6. Phylogenetic trees (ML and BI) based on the amino acid sequences of the 13 mitochondrial genes.

The bootstrap probability (the first number) and the Bayesian posterior probability (the second number) were shown at each node. The black dots mean 100/1.00. The four echinoid species newly sequenced in the present study have been used bold taxa.

Figure 7. Historical habitat of Echinoidea.

Pie charts near nodes indicated the probabilities of certain ancestral habitat. Red clades indicated the deep-sea species.