Partial Mitochondrial Gene Arrangements Support a Close Relationship between Tardigrada and Arthropoda

  • Ryu, Shi Hyun (Department of Biology, Teachers College, Kyungpook National University) ;
  • Lee, Ji Min (Department of Biology, Teachers College, Kyungpook National University) ;
  • Jang, Kuem-Hee (Department of Biology, Teachers College, Kyungpook National University) ;
  • Choi, Eun Hwa (Department of Biology, Teachers College, Kyungpook National University) ;
  • Park, Shin Ju (Department of Biology, Teachers College, Kyungpook National University) ;
  • Chang, Cheon Young (Department of Biology, College of Natural Sciences, Daegu University) ;
  • Kim, Won (School of Biological Sciences, College of Natural Sciences, Seoul National University) ;
  • Hwang, Ui Wook (Department of Biology, Teachers College, Kyungpook National University)
  • Received : 2007.04.24
  • Accepted : 2007.07.16
  • Published : 2007.12.31

Abstract

Regions (about 3.7-3.8 kb) of the mitochondrial genomes (rrnL-cox1) of two tardigrades, a heterotardigrade, Batillipes pennaki, and a eutardigrade, Pseudobiotus spinifer, were sequenced and characterized. The gene order in Batillipes was $\underline{rrnL}-\underline{V}-\underline{rrnS}-\underline{Q}-\underline{I}$-M-nad2-W-$\underline{C}-\underline{Y}$-cox1, and in Pseudobiotus it was $\underline{rrnL}-\underline{V}-\underline{rrnS}-\underline{Q}$-M-nad2-W-$\underline{C}-\underline{Y}$-cox1. With the exception of the trnI gene, the two tardigrade regions have the same gene content and order. Their gene orders are strikingly similar to that of the chelicerate Limulus polyphemus (rrnL-V-rrnS-CR-I-Q-M-nad2-W-C-Y-cox1), which is considered to be ancestral for arthropods. Although the tardigrades do not have a distinct control region (CR) within this segment, the trnI gene in Pseudobiotus is located between rrnL-trnL1 and trnL2-nad1, and the trnI gene in Batillipes is located between trnQ and trnM. In addition, the 106-bp region between trnQ and trnM in Batillipes not only contains two plausible trnI genes with opposite orientations, but also exhibits some CR-like characteristics. The mitochondrial gene arrangements of 183 other protostomes were compared. 60 (52.2%) of the 115 arthropods examined have the M-nad2-W-C-Y-cox1 arrangement, and 88 (76.5%) the M-nad2-W arrangement, as found in the tardigrades. In contrast, no such arrangement was seen in the 70 non-arthropod protostomes studied. These are the first non-sequence molecular data that support the close relationship of tardigrades and arthropods.

Keywords

Acknowledgement

Supported by : Korea Research Foundation

References

  1. Aguinaldo, A. M. A., Turbeville, J. M., Linford, L. S., Rivera, M. C., Garey, J. R., et al. (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489-493 https://doi.org/10.1038/387489a0
  2. Boore, J. L. (1999) Animal mitochondrial genomes. Nucleic Acids Res. 27, 1767-1780 https://doi.org/10.1093/nar/27.8.1767
  3. Boore, J. L. and Brown, W. M. (1998) Big trees from little genomes: mitochondrial gene order as phylogenetic tool. Curr. Opin. Genet. Dev. 8, 668-674 https://doi.org/10.1016/S0959-437X(98)80035-X
  4. Boore, J. L., Lavrov, D. V., and Brown, W. M. (1998) Gene translocation links insects and crustaceans. Nature 392, 667-668 https://doi.org/10.1038/33577
  5. Brusca, R. C. and Brusca, G. J. (2003) Invertebrates 2nd Eds., Sinauer, Associates, Sunderland, Mass
  6. Dewel, R. A. and Clark, W. H. (1973) Studies on the tardigrades. II. Fine structure of the pharynx of Milnesium tardigradum Doyere. Tiss. Cell 5, 161-169 https://doi.org/10.1016/S0040-8166(73)80013-8
  7. Folmer, O., Black, M., Hoeh, R., Lutz, R. A., and Vrijekhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294-299
  8. Garey, J. R., Krotec, M., Nelson, D. R., and Brook, J. (1996) Molecular analysis supports a tardigrade-arthropod association. Inv. Biol. 115, 79-88 https://doi.org/10.2307/3226943
  9. Giribet, G., Carranza, S., Baguñá, J., Riutort, M., and Ribera, C. (1996) First molecular evidence for the existence of a Tardigrada+ Arthropoda clade. Mol. Biol. Evol. 13, 76-84 https://doi.org/10.1093/oxfordjournals.molbev.a025573
  10. Giribet, G., Edgecombe, G. D., and Wheeler, W. C. (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413, 157-161 https://doi.org/10.1038/35093097
  11. Guidetti, R. and Bertolani, R. (2005) Tardigrade taxonomy: an updated check list of the taxa and a list of characters for their identification. Zootaxa 845, 1-46 https://doi.org/10.11646/zootaxa.845.1.1
  12. Junqueira, A. C., Lessinger, A. C., Torres, T. T., da Silva., F. R., Vettore, A. L., et al. (2004) The mitochondrial genome of the blowfly Chrysomya chloropyga (Diptera: Calliphoridae). Gene 339, 7-15 https://doi.org/10.1016/j.gene.2004.06.031
  13. Kambhampati, S. and Smith, P. T. (1995) PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol. Biol. 4, 233-236 https://doi.org/10.1111/j.1365-2583.1995.tb00028.x
  14. Kinchin, I. M. (1992) What is a tardigrade? Microscopy (London) 36, 628-634
  15. Lessinger, A. C., Junqueira, A. C., Conte, F. F., and Azeredo- Espin, A. M. (2004) Analysis of a conserved duplicated tRNA gene in the mitochondrial genome of blowflies. Gene 15, 1-6 https://doi.org/10.1016/0378-1119(81)90098-6
  16. Lim, J. T. and Hwang, U. W. (2006) The complete mitochondrial genome of Pollicipes mitella (Crustacea, Maxillopoda, Cirripedia): Non-monophylies of Maxillipoda and Crustacea. Mol. Cells 22, 314-322
  17. Lowe, T. M. and Eddy, S. R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964 https://doi.org/10.1093/nar/25.5.955
  18. Mallatt, J. M., Garey, J. R., and Shultz, J. W. (2004) Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol. Phlyogenet. Evol. 31, 178-191 https://doi.org/10.1016/j.ympev.2003.07.013
  19. Moritz, C. and Brown, W. M. (1997) Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc. Natl. Acad. Sci. USA 84, 7183-7187
  20. Nielsen, C. (2001) Animal evolution: interrelationships of the living phyla. Oxford University Press, UK
  21. Park, S. J., Lee, Y. S., and Hwang, U. W. (2007) The complete mitochondrial genome of the sea spider Achelia bituberculata (Pycnogonida, Ammotheidae): arthropod ground pattern of gene arrangement. BMC Genomics 8, 343 https://doi.org/10.1186/1471-2164-8-343
  22. Podsiadlowski, L. and Braband, A. (2006) The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida). BMC Genomics 7, 284 https://doi.org/10.1186/1471-2164-7-284
  23. Qiu, Y., Song, D., Zhou, K., and Sun, H. (2005) The mitochondrial sequences of Heptathela hangzhouensis and Ornithoctonus huwena reveal unique gene arrangements and atypical tRNAs. J. Mol. Evol. 60, 57-71 https://doi.org/10.1007/s00239-004-0010-2
  24. Rahm, G. (1937) Eine neue Tardigraden-Ordnung aus den heissen Quellen von Unzen, Inzel Kyushu, Japan. Zool. Anz. 120, 65-71
  25. Ramazzotti, G. and Maucci, W. (1983) II Phylum Tardigrada. Terza deizoine rivenduta e corretta. Me. Ist. Ital. Idrobiol. Dott. Marco Marchi. 42, 1-1012
  26. Regier, J. C. and Shultz, J. W. (2001) Elongation factor-2: A useful gene for arthropod phylogenetics. Mol. Phlyogenet. Evol. 20, 136-148 https://doi.org/10.1006/mpev.2001.0956
  27. Shao, R., Aoki, Y., Mitani, H., Tabuchi, N., Barker, S. C., et al. (2004a) The mitochondrial genomes of soft ticks have an arrangement of genes that has remained unchanged for over 400 million years. Insect Mol. Biol. 13, 219-224 https://doi.org/10.1111/j.0962-1075.2004.00447.x
  28. Shao, R., Barker, S. C., Mitani, H., Aoki, Y., and Fukunaga, M. (2004b) Evolution of duplicate control regions in the mitochondrial genomes of metazoan: A case study with Australian Ixodes ticks. Mol. Biol. Evol. 22, 620-629 https://doi.org/10.1093/molbev/msi047
  29. Sun, H., Zhou, K., and Song, D. (2005) Mitochondrial genome of the Chinese mitten crab Eriocheir japonica sinensis (Barachyura: Thoracotremata: Grapsoidea) reveals a novel gene order and two target regions of gene rearrangements. Gene 349, 207-217 https://doi.org/10.1016/j.gene.2004.12.036
  30. Von Siebold, C. T. E. (1854) In: von Siebold, C.T.E. and Stannius, H (eds), Handbuch der Zootomie. Berlin: Viet