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

PeerJ. 2022 Jul 28:10:e13730. doi: 10.7717/peerj.13730. eCollection 2022.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Genome, Mitochondrial* / genetics
  • Phylogeny
  • RNA, Transfer / genetics
  • Sea Urchins / genetics

Substances

  • RNA, Transfer

Grants and funding

This study was supported by research grants from the Key Research Program of Frontier Sciences, the Chinese Academy of Sciences (QYZDB-SSWDQC036), the National Science Foundation for Distinguished Young Scholars (42025603), and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB42000000). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.