Abstract
The complete nucleotide sequence of the 14,017-bp mitochondrial (mt) genome of the articulate brachiopod Laqueus rubellus is presented. Being one of the smallest of known mt genomes, it has an extremely compact gene organization. While the same 13 polypeptides, two rRNAs, and 22 tRNAs are encoded as in most other animal mtDNAs, lengthy noncoding regions are absent, with the longest apparent intergenic sequence being 54 bp in length. Gene-end sequence overlaps are prevalent, and several stop codons are abbreviated. The genes are generally shorter, and three of the protein-coding genes are the shortest among known homologues. All of the tRNA genes indicate size reduction in either or both of the putative TPsiC and DHU arms compared with standard tRNAs. Possession of a TV (TPsiC arm-variable loop) replacement loop is inferred for tRNA(R) and tRNA(L-tag). The DHU arm appears to be unpaired not only in tRNA(S-tct) and tRNA(S-tga), but also in tRNA(C), tRNA(I), and tRNA(T), a novel condition. All the genes are encoded in the same DNA strand, which has a base composition rich in thymine and guanine. The genome has an overall gene arrangement drastically different from that of any other organisms so far reported, but contains several short segments, composed of 2-3 genes, which are found in other mt genomes. Combined cooccurrence of such gene assortments indicates that the Laqueus mt genome is similar to the annelid Lumbricus, the mollusc Katharina, and the octocoral Sarcophyton mt genomes, each with statistical significance. Widely accepted schemes of metazoan phylogeny suggest that the similarity with the octocoral could have arisen through a process of convergent evolution, while it appears likely that the similarities with the annelid and the mollusc reflect phylogenetic relationships.
Full Text
The Full Text of this article is available as a PDF (340.6 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
- Asakawa S., Himeno H., Miura K., Watanabe K. Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics. 1995 Jul;140(3):1047–1060. doi: 10.1093/genetics/140.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Asakawa S., Kumazawa Y., Araki T., Himeno H., Miura K., Watanabe K. Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol. 1991 Jun;32(6):511–520. doi: 10.1007/BF02102653. [DOI] [PubMed] [Google Scholar]
- Barnes W. M. PCR amplification of up to 35-kb DNA with high fidelity and high yield from lambda bacteriophage templates. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2216–2220. doi: 10.1073/pnas.91.6.2216. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beagley C. T., Okimoto R., Wolstenholme D. R. The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, and a near-standard genetic code. Genetics. 1998 Mar;148(3):1091–1108. doi: 10.1093/genetics/148.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beaton M. J., Roger A. J., Cavalier-Smith T. Sequence analysis of the mitochondrial genome of Sarcophyton glaucum: conserved gene order among octocorals. J Mol Evol. 1998 Dec;47(6):697–708. doi: 10.1007/pl00006429. [DOI] [PubMed] [Google Scholar]
- Boore J. L., Brown W. M. Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics. 1994 Oct;138(2):423–443. doi: 10.1093/genetics/138.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boore J. L., Collins T. M., Stanton D., Daehler L. L., Brown W. M. Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature. 1995 Jul 13;376(6536):163–165. doi: 10.1038/376163a0. [DOI] [PubMed] [Google Scholar]
- Boore J. L., Lavrov D. V., Brown W. M. Gene translocation links insects and crustaceans. Nature. 1998 Apr 16;392(6677):667–668. doi: 10.1038/33577. [DOI] [PubMed] [Google Scholar]
- Cantatore P., Roberti M., Rainaldi G., Gadaleta M. N., Saccone C. The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J Biol Chem. 1989 Jul 5;264(19):10965–10975. [PubMed] [Google Scholar]
- Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
- Crozier R. H., Crozier Y. C. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics. 1993 Jan;133(1):97–117. doi: 10.1093/genetics/133.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Desjardins P., Morais R. Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol. 1990 Apr 20;212(4):599–634. doi: 10.1016/0022-2836(90)90225-B. [DOI] [PubMed] [Google Scholar]
- Field K. G., Olsen G. J., Lane D. J., Giovannoni S. J., Ghiselin M. T., Raff E. C., Pace N. R., Raff R. A. Molecular phylogeny of the animal kingdom. Science. 1988 Feb 12;239(4841 Pt 1):748–753. doi: 10.1126/science.3277277. [DOI] [PubMed] [Google Scholar]
- Halanych K. M., Bacheller J. D., Aguinaldo A. M., Liva S. M., Hillis D. M., Lake J. A. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science. 1995 Mar 17;267(5204):1641–1643. doi: 10.1126/science.7886451. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
- Jacobs H. T., Asakawa S., Araki T., Miura K., Smith M. J., Watanabe K. Conserved tRNA gene cluster in starfish mitochondrial DNA. Curr Genet. 1989 Mar;15(3):193–206. doi: 10.1007/BF00435506. [DOI] [PubMed] [Google Scholar]
- Jacobs H. T., Elliott D. J., Math V. B., Farquharson A. Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol. 1988 Jul 20;202(2):185–217. doi: 10.1016/0022-2836(88)90452-4. [DOI] [PubMed] [Google Scholar]
- Janke A., Feldmaier-Fuchs G., Thomas W. K., von Haeseler A., Päbo S. The marsupial mitochondrial genome and the evolution of placental mammals. Genetics. 1994 May;137(1):243–256. doi: 10.1093/genetics/137.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kumazawa Y., Nishida M. Variations in mitochondrial tRNA gene organization of reptiles as phylogenetic markers. Mol Biol Evol. 1995 Sep;12(5):759–772. doi: 10.1093/oxfordjournals.molbev.a040254. [DOI] [PubMed] [Google Scholar]
- Mitchell S. E., Cockburn A. F., Seawright J. A. The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. Genome. 1993 Dec;36(6):1058–1073. doi: 10.1139/g93-141. [DOI] [PubMed] [Google Scholar]
- Okimoto R., Macfarlane J. L., Clary D. O., Wolstenholme D. R. The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics. 1992 Mar;130(3):471–498. doi: 10.1093/genetics/130.3.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pont-Kingdon G., Okada N. A., Macfarlane J. L., Beagley C. T., Watkins-Sims C. D., Cavalier-Smith T., Clark-Walker G. D., Wolstenholme D. R. Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homologue of bacterial MutS: a possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol. 1998 Apr;46(4):419–431. doi: 10.1007/pl00006321. [DOI] [PubMed] [Google Scholar]
- Päbo S., Thomas W. K., Whitfield K. M., Kumazawa Y., Wilson A. C. Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol. 1991 Nov;33(5):426–430. doi: 10.1007/BF02103134. [DOI] [PubMed] [Google Scholar]
- Ramón Valverde J., Batuecas B., Moratilla C., Marco R., Garesse R. The complete mitochondrial DNA sequence of the crustacean Artemia franciscana. J Mol Evol. 1994 Oct;39(4):400–408. doi: 10.1007/BF00160272. [DOI] [PubMed] [Google Scholar]
- Smith M. J., Arndt A., Gorski S., Fajber E. The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol. 1993 Jun;36(6):545–554. doi: 10.1007/BF00556359. [DOI] [PubMed] [Google Scholar]
- Stechmann A., Schlegel M. Analysis of the complete mitochondrial DNA sequence of the brachiopod terebratulina retusa places Brachiopoda within the protostomes. Proc Biol Sci. 1999 Oct 22;266(1433):2043–2052. doi: 10.1098/rspb.1999.0885. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolstenholme D. R. Animal mitochondrial DNA: structure and evolution. Int Rev Cytol. 1992;141:173–216. doi: 10.1016/s0074-7696(08)62066-5. [DOI] [PubMed] [Google Scholar]
- Wolstenholme D. R., Macfarlane J. L., Okimoto R., Clary D. O., Wahleithner J. A. Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1324–1328. doi: 10.1073/pnas.84.5.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamazaki N., Ueshima R., Terrett J. A., Yokobori S., Kaifu M., Segawa R., Kobayashi T., Numachi K., Ueda T., Nishikawa K. Evolution of pulmonate gastropod mitochondrial genomes: comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. Genetics. 1997 Mar;145(3):749–758. doi: 10.1093/genetics/145.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]