Giant group I intron in a mitochondrial genome is removed by RNA back-splicing

Abstract

<p><i>Background - </i>The mitochondrial genomes of mushroom corals (Corallimorpharia) are remarkable for harboring two complex group I introns; ND5-717 and COI-884. How these autocatalytic RNA elements interfere with mitochondrial RNA processing is currently not known. Here, we report experimental support for unconventional processing events of ND5-717 containing RNA. <p><i>Results - </i>We obtained the complete mitochondrial genome sequences and corresponding mitochondrial transcriptomes of the two distantly related corallimorpharian species <i>Ricordea yuma</i> and <i>Amplexidiscus fenestrafer</i>. All mitochondrial genes were found to be expressed at the RNA-level. Both introns were perfectly removed by autocatalytic splicing, but COI-884 excision appeared more efficient than ND5-717. ND5-717 was organized into giant group I intron elements of 18.1 kb and 19.3 kb in <i>A. fenestrafer</i> and <i>R. yuma</i>, respectively. The intron harbored almost the entire mitochondrial genome embedded within the P8 peripheral segment. <p><i>Conclusion - </i>ND5-717 was removed by group I intron splicing from a small primary transcript that contained a permutated intron–exon arrangement. The splicing pathway involved a circular exon-containing RNA intermediate, which is a hallmark of RNA back-splicing. ND5-717 represents the first reported natural group I intron that becomes excised by back-splicing from a permuted precursor RNA. Back-splicing may explain why Corallimorpharia mitochondrial genomes tolerate giant group I introns.