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Mitochondrial genome rearrangement in a hydrothermal vent-endemic lineage of provannid gastropods provides a new DNA marker for phylogeographical studies

Published online by Cambridge University Press:  21 November 2012

Hiroka Hidaka ,
Hiromi Watanabe ,
Yasunori Kano  and
Shigeaki Kojima
Hiroka Hidaka
Affiliation:
Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8561, Japan Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
Hiromi Watanabe
Affiliation:
Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Yasunori Kano
Affiliation:
Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
Shigeaki Kojima*
Affiliation:
Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8561, Japan Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
*
Correspondence should be addressed to: S. Kojima, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan email: [email protected]
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Abstract

The nucleotide sequences of mitochondrial DNA fragments containing genes for cytochrome c oxidase subunits I and II, ATPase subunits 6 and 8, large and small subunits of rRNA, and 9 tRNAs were determined using 2 genetically distinct representative specimens of the hydrothermal vent-endemic genus, Alviniconcha, and for the hydrothermal vent-endemic species, Ifremeria nautilei (Provannidae: Caenogastropoda: Mollusca). All 3 specimens showed tRNATrp gene translocation. To determine the time point at which this translocation occurred, we determined the nucleotide sequences of fragments containing 7 tRNA genes for another 3 Alviniconcha and 2 Ifremeria specimens, as well as for 7 related species. Our findings indicated that the translocation occurred in a common ancestor of the Alviniconcha and Ifremeria genera. Relatively long non-coding regions were observed on both sides of the tRNATrp gene and at the original position of this gene in all the Alviniconcha and Ifremeria gastropod specimens. Overall, the mitochondrial non-coding regions appear to provide much more information about genetic structure than the mitochondrial COI gene does and could therefore be a valuable marker for future studies.

Keywords

mitochondrial genomerearrangementprovannidAlviniconcha spp.Ifremeria nautileihydrothermal vent
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 4 , June 2013 , pp. 1053 - 1058
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012 

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References

REFERENCES

Arrieta, J.M., Arnaud-Haond, S. and Duarte, C.M. (2010) What lies underneath: conserving the oceans' genetic resources. Proceedings of the National Academy of Sciences of the United States of America 107, 18318–18324.CrossRefGoogle ScholarPubMed
Bandelt, H.J., Forster, P. and Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Boore, J.L. and Brown, W.M. (1998) Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Current Opinion in Genetics and Development 8, 668–674.CrossRefGoogle ScholarPubMed
Cunha, R.L., Grande, C. and Zardoya, R. (2009) Neogastropod phylogenetic relationships based on entire mitochondrial genomes. BMC Evolutionary Biology 9, 210.CrossRefGoogle ScholarPubMed
Endo, K., Noguchi, Y., Ueshima, R. and Jacobs, H.T. (2005) Novel repetitive structures, deviant protein-encoding sequences and unidentified ORFs in the mitochondrial genome of the brachiopod Lingula anatina. Journal of Molecular Evolution 61, 36–53.CrossRefGoogle ScholarPubMed
Excoffier, L. and Lischer, H.E.L. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Grande, C., Templado, J. and Zardoya, R. (2008) Evolution of gastropod mitochondrial genome arrangements. BMC Evolutionary Biology 8, 6.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R.A. and Vrijenhoek, R.C. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Gamo, T., Sakai, H., Ishibashi, J., Nakayama, E., Isshiki, K., Matsuura, H., Shitashima, K., Takeuchi, K. and Ohta, S. (1993) Hydrothermal plumes in the eastern Manus Basin, Bismarck Sea: CH4, Mn, Al and ph anomalies. Deep-Sea Research Part I 40, 2335–2349.CrossRefGoogle Scholar
Hasegawa, T., Yamaguchi, T., Kojima, S. and Ohta, S. (1996) Phylogenetic analysis among three species of intertidal barnacles of the genus Tetraclita (Cirripedia: Balanomorpha) by nucleotide sequences of a mitochondrial gene. Benthos Research 51, 33–39. [In Japanese with English abstract.]CrossRefGoogle Scholar
Ishibashi, J., Luption, E., Yamaguchi, T., Querellou, J., Nunoura, T. and Takai, K. (2006) Expedition reveals changes in Lau Basin hydrothermal system. EOS Transactions, American Geophysical Union 87, 13–17.CrossRefGoogle Scholar
Johnson, S.B., Warén, A., Lee, R.W., Kano, Y., Kaim, A., Davis, A., Strong, E.E. and Vrijenhoek, R.C. (2010) Rubyspira, a new genus and two new species of bone-eating deep-sea snails with ancient habits. Biological Bulletin. Marine Biological Laboratory, Woods Hole 219, 166–177.CrossRefGoogle ScholarPubMed
Kojima, S. (2010) Extensive mitochondrial genome rearrangements between Cerithioidea and Hypsogastropoda (Mollusca; Caenogastropoda) as determined from the partial nucleotide sequences of the mitochondrial DNA of Cerithidea djadjariensis and Batillaria cumingi. Zoological Science 27, 494–498.CrossRefGoogle ScholarPubMed
Kojima, S., Segawa, R., Fujiwara, Y., Hashimoto, J. and Ohta, S. (2000) Genetic differentiation of populations of a hydrothermal vent-endemic gastropod, Ifremeria nautilei, between the North Fiji Basin and the Manus Basin revealed by nucleotide sequences of mitochondrial DNA. Zoological Science 17, 1167–1174.CrossRefGoogle ScholarPubMed
Kojima, S., Segawa, R., Fujiwara, Y., Fujikura, K., Ohta, S. and Hashimoto, J. (2001) Phylogeny of hydrothermal vent-endemic gastropods Alviniconcha spp. from the Western Pacific revealed by mitochondrial DNA sequences. Biological Bulletin. Marine Biological Laboratory, Woods Hole 200, 298–304.CrossRefGoogle ScholarPubMed
Kojima, S., Fujikura, K., Okutani, T. and Hashimoto, J. (2004) Phylogenetic status of Alviniconcha gastropods from the Indian Ocean (Provannidae: Mollusca) revealed by nucleotide sequences of mitochondrial DNA. Venus 63, 65–68.Google Scholar
Le, T.H., Blair, D., Agatsuma, T., Humair, P.F., Campbell, N.J., Iwagami, M., Littlewood, D.T., Peacock, B., Johnston, D.A., Bartley, J., Rollinson, D., Herniou, E.A., Zarlenga, D.S. and McManus, D.P. (2000) Phylogenies inferred from mitochondrial gene orders—a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 1123–1125.CrossRefGoogle ScholarPubMed
Lowe, T.M. and Eddy, S.R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25, 955–964.CrossRefGoogle ScholarPubMed
Löytynoja, A. and Milinkovitch, M.C. (2003) A hidden Markov model for progressive multiple alignment. Bioinformatics 19, 913–922.CrossRefGoogle ScholarPubMed
Nei, M. (1987) Molecular evolutionary genetics. New York: Columbia University Press.CrossRefGoogle Scholar
Nojiri, Y., Ishibashi, J., Kawai, T., Otsuki, A. and Sakai, H. (1989) Hydrothermal plumes along the North Fiji Basin spreading axis. Nature 342, 667–670.CrossRefGoogle Scholar
Pearson, W.R. and Lipman, D.J. (1988) Improved tools for biological sequence comparison. Proceedings of the National Academy of Sciences of the United States of America 85, 2444–2448.CrossRefGoogle ScholarPubMed
Ponder, W.F., Colgan, D.J., Healy, J.M., Nützel, A., Simone, L.R.L. and Strong, E.E. (2008) Caenogastropoda. In Ponder, W.F. and Lindberg, D.R. (eds) Phylogeny and evolution of the Mollusca. Berkeley, CA: University of California Press, pp. 331–383.Google Scholar
Rawlings, T.A., MacInnis, M.J., Bieler, R., Boore, J.L. and Collins, T.M. (2010) Sessile snails, dynamic genomes: gene rearrangements within the mitochondrial genome of a family of caenogastropod molluscs. BMC Genomics 11, 440.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Sasaki, T., Warén, A., Kano, Y., Okutani, T. and Fujikura, K. (2010) Gastropods from recent hot vent and cold seeps: systematics, diversity and life strategies. In Kiel, S. (ed.) The vent and seep biota, topics in geobiology 33. Dordrecht, The Netherlands: Springer, pp. 169–254.CrossRefGoogle Scholar
Suzuki, Y., Kojima, S., Sasaki, T., Suzuki, M., Utsumi, T., Watanabe, H., Urakawa, H., Tsuchida, S., Nunoura, T., Hirayama, H., Takai, K., Nealson, K.H. and Horikoshi, K. (2006a) Host–symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Applied and Environmental Microbiology 72, 1388–1393.CrossRefGoogle ScholarPubMed
Suzuki, Y., Kojima, S., Watanabe, H., Suzuki, M., Tsuchida, S., Nunoura, T., Hirayama, H., Takai, K., Nealson, K.H. and Horikoshi, K. (2006b) Single host and symbiont lineages of hydrothermal vent gastropods of the genus Ifremeria (Provannidae): biogeography and evolution. Marine Ecology Progress Series 315, 167–175.CrossRefGoogle Scholar
Tajima, F. (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460.CrossRefGoogle ScholarPubMed
Tamaki, K. and Honza, E. (1991) Global tectonics and formation of marginal basins: role of the western Pacific. Episodes 14, 224–230.CrossRefGoogle Scholar
Van Dover, C.L. (2011) Mining seafloor massive sulphides and biodiversity: what is at risk? ICES Journal of Marine Science 68, 341–348.CrossRefGoogle Scholar
Vrijenhoek, R.C. (2010) Genetic diversity and connectivity of deep-sea hydrothermal vent metapopulations. Molecular Ecology 19, 4391–4411.CrossRefGoogle ScholarPubMed
Wilke, T. (2003) Salenthydrobia gen. nov. (Rissooidea: Hydrobiidae): a potential relic of the Messinian salinity crisis. Zoological Journal of the Linnean Society 137, 319–336.CrossRefGoogle Scholar
Willing, C.S., Mill, P.J. and Grahame, J. (1999) Partial sequence of mitochondrial genome of Littorina saxatilis: relevance to gastropod phylogenetics. Journal of Molecular Evolution 48, 348–359.CrossRefGoogle Scholar