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Novel Repetitive Structures, Deviant Protein-Encoding Sequences andUnidentified ORFs in the Mitochondrial Genome of the BrachiopodLingula anatina

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Abstract

Complete sequence determination of the brachiopod Lingula anatina mtDNA (28,818 bp) revealed an organization that is remarkably atypical for an animal mt-genome. In addition to the usual set of 37 animal mitochondrial genes, which make up only 57% (16,555 bp) of the entire sequence, the genome contains lengthy unassigned sequences. All the genes are encoded in the same DNA strand, generally in a compact way, whereas the overall gene order is highly divergent in comparison with known animal mtDNA. Individual genes are generally longer and deviate considerably in sequence from their homologues in other animals. The genome contains two major repeat regions, in which 11 units of unassigned sequences and six genes (atp8, trnM, trnQ, trnV, and part of cox2 and nad2) are found in repetition, in the form of nested direct repeats of unparalleled complexity. One of the repeat regions contains unassigned repeat units dispersed among several unique sequences, novel repetitive structure for animal mtDNAs. Each of those unique sequences contains an open reading frame for a polypeptide between 80 and 357 amino acids long, potentially encoding a functional molecule, but none of them has been identified with known proteins. In both repeat regions, tRNA genes or tRNA gene-like sequences flank major repeated units, supporting the view that those structures play a role in the mitochondrial gene rearrangements. Although the intricate repeated organization of this genome can be explained by recurrent tandem duplications and subsequent deletions mediated by replication errors, other mechanisms, such as nonhomologous recombinations, appear to explain certain structures more easily.

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Acknowledgments

This work was carried out at Glasgow University (Department of Genetics), Tsukuba University (Institute of Biological Sciences), and Tokyo University (Department of Earth and Planetary Science). We thank colleagues in those institutions for their kind support. Gordon Curry, Bernard Cohen, Tomowo Ozawa, Sohail Qureshi, Abdellatif El Meziane, and other members of the Howy lab are thanked for their advice and discussion at earlier stages of this study. We are indebted to the late professor Juichi Yanagida for his help in sample collection. This work was partly funded by grants from the Ministry of Education, Science, Sports and Culture of Japan.

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Authors and Affiliations

  1. Institute of Geoscience, University of Tsukuba, Tsukuba , 305-8572, Japan

    Kazuyoshi Endo

  2. Institute of Biological Sciences, University of Tsukuba, Tsukuba, 305-0006, Japan

    Yasuhiro Noguchi

  3. Department of Biological Sciences, University of Tokyo, Tokyo, 113-0033, Japan

    Rei Ueshima

  4. Institute of Medical Technology and Tampere University Hospital, University of Tampere, Tampere, FIN-33104, Finland

    Howard T. Jacobs

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  1. Kazuyoshi Endo
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Correspondence to Kazuyoshi Endo.

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Endo, K., Noguchi, Y., Ueshima, R. et al. Novel Repetitive Structures, Deviant Protein-Encoding Sequences andUnidentified ORFs in the Mitochondrial Genome of the BrachiopodLingula anatina. J Mol Evol 61, 36–53 (2005). https://doi.org/10.1007/s00239-004-0214-5

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