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, 11 (1), 29-40

Mitogenomics Reveals a Novel Genetic Code in Hemichordata

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Mitogenomics Reveals a Novel Genetic Code in Hemichordata

Yuanning Li et al. Genome Biol Evol.

Abstract

The diverse array of codon reassignments demonstrate that the genetic code is not universal in nature. Exploring mechanisms underlying codon reassignment is critical for understanding the evolution of the genetic code during translation. Hemichordata, comprising worm-like Enteropneusta and colonial filter-feeding Pterobranchia, is the sister taxon of echinoderms and is more distantly related to chordates. However, only a few hemichordate mitochondrial genomes have been sequenced, hindering our understanding of mitochondrial genome evolution within Deuterostomia. In this study, we sequenced four mitochondrial genomes and two transcriptomes, including representatives of both major hemichordate lineages and analyzed together with public available data. Contrary to the current understanding of the mitochondrial genetic code in hemichordates, our comparative analyses suggest that UAA encodes Tyr instead of a "Stop" codon in the pterobranch lineage Cephalodiscidae. We also predict that AAA encodes Lys in pterobranch and enteropneust mitochondrial genomes, contradicting the previous assumption that hemichordates share the same genetic code with echinoderms for which AAA encodes Asn. Thus, we propose a new mitochondrial genetic code for Cephalodiscus and a revised code for enteropneusts. Moreover, our phylogenetic analyses are largely consistent with previous phylogenomic studies. The only exception is the phylogenetic position of the enteropneust Stereobalanus, whose placement as sister to all other described enteropneusts. With broader taxonomic sampling, we provide evidence that evolution of mitochondrial gene order and genetic codes in Hemichordata are more dynamic than previously thought and these findings provide insights into mitochondrial genome evolution within this clade.

Figures

F<sc>ig</sc>. 1.—
Fig. 1.—
Variant codes in mitochondrial genomes within deuterostomes and photos from representatives of hemichordates. (A) Phylogenetic relationships according to the current understanding of deuterostome phylogeny based on multiple studies, red bars show codon reassignment events, the table on the top left shows standard genetic code for the affected codons. (B) Acorn worm Schizocardium braziliense collected from Mississippi (photo by Joie Cannon). (C) Cephalodiscus sp. collected from Heron Island, Queensland, Australia (photo by Kevin Kocot).
F<sc>ig</sc>. 2.
Fig. 2.
—Mitochondrial gene order within deuterostomes. (A) Current understanding of relationships within Deuterostomia and mitochondrial gene order for each taxon. Deuterostome phylogeny is depicted based on Cannon et al. (2014). Only protein-coding genes and ribosomal RNA genes of available mitochondrial genomes are included. Gene orders of tunicates were excluded. Genes are not scaled to real length and are indicated by standard abbreviations. Genes in a different line indicate different coding strand and colors indicate by protein complexes, and arrows indicate alternative gene arrangements in the corresponding species. (B) Hypothetical ground pattern of deuterostome mitochondrial genome. (C) Hypothetical ground pattern of hemichordate mitochondrial genome.
F<sc>ig</sc>. 3.
Fig. 3.
—Phylogenetic reconstruction of Hemichordata based on 13 mitochondrial protein-coding genes. Majority rule (50%) consensus phylogram from the Bayesian analysis of the concatenated data matrix is shown. Values are shown next to nodes with ML bootstrap support values left and posterior probabilities right. All nodes are supported with 100% bootstrap value or posterior probabilities of 1.0 unless otherwise noted.
F<sc>ig</sc>. 4.—
Fig. 4.—
Partial alignment of conserved region of translated cox1 gene sequences (100 amino acid positions) indicates that UAA decodes Tyr instead of Stop in Cephalodiscus mitochondrial genomes (confirmed by mitochondrial gene in the transcriptomic data from the same species). The alignment corresponding to amino acid positions is labeled in the header of each sequence. Codon UAA is translated into either Stop (*) based on Echinodermata codon table (Codon 9) or Tyr in Cephalodiscus mitochondrial genomes (Codon “Cepha”). The header of the sequence (Left) starting with “MT” indicates that the corresponding sequence is from mitochondrial genome assemblies, whereas “TRI” indicates that the sequence is extracted from transcriptomic data.

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