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First Complete Mitochondrial Genome Sequence From a Box Jellyfish Reveals a Highly Fragmented Linear Architecture and Insights Into Telomere Evolution

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First Complete Mitochondrial Genome Sequence From a Box Jellyfish Reveals a Highly Fragmented Linear Architecture and Insights Into Telomere Evolution

David Roy Smith et al. Genome Biol Evol.

Abstract

Animal mitochondrial DNAs (mtDNAs) are typically single circular chromosomes, with the exception of those from medusozoan cnidarians (jellyfish and hydroids), which are linear and sometimes fragmented. Most medusozoans have linear monomeric or linear bipartite mitochondrial genomes, but preliminary data have suggested that box jellyfish (cubozoans) have mtDNAs that consist of many linear chromosomes. Here, we present the complete mtDNA sequence from the winged box jellyfish Alatina moseri (the first from a cubozoan). This genome contains unprecedented levels of fragmentation: 18 unique genes distributed over eight 2.9- to 4.6-kb linear chromosomes. The telomeres are identical within and between chromosomes, and recombination between subtelomeric sequences has led to many genes initiating or terminating with sequences from other genes (the most extreme case being 150 nt of a ribosomal RNA containing the 5' end of nad2), providing evidence for a gene conversion-based model of telomere evolution. The silent-site nucleotide variation within the A. moseri mtDNA is among the highest observed from a eukaryotic genome and may be associated with elevated rates of recombination.

Figures

F<sc>IG</sc>. 1.—
FIG. 1.—
Mitochondrial genome architectural diversity within Medusozoa. (A and B) Genetic maps of completely sequenced medusozoan mtDNAs. The genomic AT content and coding composition are indicated next to the taxon name. mtDNA lengths are shown adjacent to the mitochondrial chromosomes (Chr). Synteny between the mtDNA of Alatina moseri and that of Aurelia aurita is marked with horizontal black lines, which have labels corresponding to A. moseri chromosome numbers. See figure 2 for details on the A. moseri mtDNA pseudogenes. (C) Hypotheses on the evolution of medusozoan mtDNA architecture. Phylogenetic relationships based on Collins et al. (2006, and Cartwright et al. (2008). Note: cnidarian mtDNA protein-coding genes are translated using the minimally derived genetic code (UAG = Tryptophan).
F<sc>IG</sc>. 2.—
FIG. 2.—
Alignment and architecture of the Alatina moseri mitochondrial telomeric and subtelomeric regions. The Alatina moseri mitochondrial genome is divided into eight chromosomes (Chr), each of which has two telomeres: left and right (based on genetic map in fig. 1A). The telomeres (turquoise; length = 750 nt; not to scale) are identical in sequence and found in opposing orientations so that they make up an IR. The subtelomeric regions are composed of coding (dark blue) and noncoding (black) regions and contain fragments of genes (red) from neighboring chromosomes. Gray highlighting denotes sequence identity between different subtelomeric regions; when the sequence identity includes coding DNA, these regions are striped.

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