Sea anemones possess dynamic mitogenome structures

• Published in: Molecular phylogenetics and evolution 2014-06, Vol.75, p.184-193
• Main Authors: Emblem, Åse, Okkenhaug, Siri, Weiss, Emily S., Denver, Dee R., Karlsen, Bård Ove, Moum, Truls, Johansen, Steinar D.
• Format: Article
• Language: English
• Subjects: Animals; Base Sequence; Biological Evolution; DNA Transposable Elements; DNA, Mitochondrial - genetics; Genome, Mitochondrial; Group I intron; Hexacorallia; High-Throughput Nucleotide Sequencing; Homing endonuclease gene; Introns; Marine; Mitochondrial genome; Molecular Sequence Data; Mutagenesis, Insertional; Nucleic Acid Conformation; Phylogeny; Pyrosequencing; Sea Anemones - genetics; Sequence Analysis, DNA; SOLiD ligation sequencing
• ISSN: 1055-7903; 1095-9513
• DOI: 10.1016/j.ympev.2014.02.016

[Display omitted] •We present genomic resources of cold-water sea anemones.•An obligatory group I intron contains truncated duplicated gene sequences.•A mobile group I intron contains an expressed homing endonuclease gene.•We detect a novel insertion element that contains expressed protein coding genes.•Introns and insertion element have higher substitution rates. A notable feature of hexacoral mitogenomes is the presence of complex self-catalytic group I introns. We investigated mitogenome structural variations and evolutionary mechanisms in actiniarian sea anemones based on the complete mitogenome sequence of the cold-water sea anemone species Urticina eques, Bolocera tuediae, Hormathia digitata and Metridium senile, and two isolates of the sub-tropical Aiptasia pulchella. Whole genome sequencing at 50 times coverage of B. tuediae and H. digitata indicated low mtDNA copy number of per haploid nuclear genome and presence of rare haplotypes. A group I intron inserted in ND5 was found to host essential mitochondrial protein genes in all species, and an additional truncated copy of ND5 in B. tuediae. A second group I intron (inserted in COI) that contained a homing endonuclease gene (HEG) was present in all mtDNA examined. Different variants of HEGs were observed, and included expressed elements fused in-frame with upstream exons and free-standing HEGs embedded within the intron. A notable hallmark of HEGs was a high extent of overlap with ribozyme structural elements; the U. eques HEG overlapped with the entire intron. We reconstructed the evolutionary history of the COI intron from insertion at unoccupied cognate sites, through HEG degradation, to intron loss. We also identified a novel insertion element in U. eques that contained two expressed protein-coding genes. An evolutionary analysis of the sea anemone mtDNA genes revealed higher substitution rates in the HEG and the insertion sequence as compared to the other loci, indicating relaxed selective pressures in these elements. We conclude that sea anemone mitogenomes are surprisingly dynamic in structure despite the economical organization and low sequence mutation rate.