Separate Origins of Group I Introns in Two Mitochondrial Genes of the Katablepharid Leucocryptos marina

Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan.
PLoS ONE (Impact Factor: 3.23). 05/2012; 7(5):e37307. DOI: 10.1371/journal.pone.0037307
Source: PubMed


Mitochondria are descendants of the endosymbiotic α-proteobacterium most likely engulfed by the ancestral eukaryotic cells, and the proto-mitochondrial genome should have been severely streamlined in terms of both genome size and gene repertoire. In addition, mitochondrial (mt) sequence data indicated that frequent intron gain/loss events contributed to shaping the modern mt genome organizations, resulting in the homologous introns being shared between two distantly related mt genomes. Unfortunately, the bulk of mt sequence data currently available are of phylogenetically restricted lineages, i.e., metazoans, fungi, and land plants, and are insufficient to elucidate the entire picture of intron evolution in mt genomes. In this work, we sequenced a 12 kbp-fragment of the mt genome of the katablepharid Leucocryptos marina. Among nine protein-coding genes included in the mt genome fragment, the genes encoding cytochrome b and cytochrome c oxidase subunit I (cob and cox1) were interrupted by group I introns. We further identified that the cob and cox1 introns host open reading frames for homing endonucleases (HEs) belonging to distantly related superfamilies. Phylogenetic analyses recovered an affinity between the HE in the Leucocryptos cob intron and two green algal HEs, and that between the HE in the Leucocryptos cox1 intron and a fungal HE, suggesting that the Leucocryptos cob and cox1 introns possess distinct evolutionary origins. Although the current intron (and intronic HE) data are insufficient to infer how the homologous introns were distributed to distantly related mt genomes, the results presented here successfully expanded the evolutionary dynamism of group I introns in mt genomes.

Download full-text


Available from: Ryoma Kamikawa
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Mitochondria are membrane-enclosed organelles present in most eukaryotic cells that generate most of the cell's adenosine triphosphate (ATP) supply. Derived from a proteobacterial ancestor, mitochondria harbour their own, drastically reduced genome. Starting from a prokaryote-like ancestral state encoding a complete ribosomal ribonucleic acid (rRNA) operon, a complete set of transfer RNAs (tRNAs) required for translation, and key enzymes of the respiratory chain as well as some ribosomal proteins, the mitogenome has been dramatically restructured and further reduced in many of the eukaryotic lineages. The loss and transfer to the nucleus of mitochondrial genes is a common trend in most phyla, in particular in Metazoa and Alveolata. In extreme, phylogenetically dispersed cases, often associated with parasitic or anaerobic life styles, mitochondria have been transformed to the so-called mitosomes or hydrogenosomes devoid of their own genetic material. Ancestrally a single circular deoxyribonucleic acid (DNA), mitogenomes have evolved to complex, fragmented architectures in particular in Euglenozoa.
    Full-text · Chapter · Sep 2013
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Mitochondrial (mt) genome sequences, which often bear introns, have been sampled from phylogenetically diverse eukaryotes. Thus, we can anticipate novel insights into intron evolution from previously unstudied mt genomes. We here investigated the origins and evolution of three introns in the mt genome of the haptophyte Chrysochromulina sp. NIES-1333, which was sequenced completely in this study. All the three introns were characterized as group II, on the basis of predicted secondary structure, and the conserved sequence motifs at the 5' and 3' termini. Our comparative studies on diverse mt genomes prompt us to propose that the Chrysochromulina mt genome laterally acquired the introns from mt genomes in distantly related eukaryotes. Many group II introns harbor intronic open reading frames for the proteins (intron-encoded proteins or IEPs), which likely facilitate the splicing of their host introns. However, we propose that a "free-standing," IEP-like protein, which is not encoded within any introns in the Chrysochromulina mt genome, is involved in the splicing of the first cox1 intron that lacks any open reading frames.
    Full-text · Article · May 2014