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Characterization of the mitochondrial genome of Diphyllobothrium latum (Cestoda: Pseudophyllidea) – implications for the phylogeny of eucestodes

Published online by Cambridge University Press:  11 January 2007

J.-K. PARK ,
K.-H. KIM ,
S. KANG ,
H. K. JEON ,
J.-H. KIM ,
D. T. J. LITTLEWOOD  and
K. S. EOM
J.-K. PARK*
Affiliation:
Department of Parasitology, College of Medicine, Chungbuk National University Cheongju, Chungbuk 361-763, Republic of Korea
K.-H. KIM
Affiliation:
Department of Parasitology, College of Medicine, Chungbuk National University Cheongju, Chungbuk 361-763, Republic of Korea Present address: Korea Food and Drug Administration, Seoul 122-704, Republic of Korea.
S. KANG
Affiliation:
Department of Parasitology, College of Medicine, Chungbuk National University Cheongju, Chungbuk 361-763, Republic of Korea
H. K. JEON
Affiliation:
Department of Parasitology, College of Medicine, Chungbuk National University Cheongju, Chungbuk 361-763, Republic of Korea
J.-H. KIM
Affiliation:
Faculty of Marine Bioscience and Technology, Kangnung National University, Kangnung City, Kangwon-do 210-702, Republic of Korea
D. T. J. LITTLEWOOD
Affiliation:
Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
K. S. EOM
Affiliation:
Department of Parasitology, College of Medicine, Chungbuk National University Cheongju, Chungbuk 361-763, Republic of Korea
*
*Corresponding author: Department of Parasitology, College of Medicine, Chungbuk National University Cheongju, Chungbuk 361-763, Republic of Korea. Tel: 82 43 261 2843. Fax: 82 43 272 1603. E-mail: jkpyou@chungbuk.ac.kr
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Summary

The complete nucleotide sequence of the mitochondrial genome was determined for the fish tapeworm Diphyllobothrium latum. This genome is 13 608 bp in length and encodes 12 protein-coding genes (but lacks the atp8), 22 transfer RNA (tRNA) and 2 ribosomal RNA (rRNA) genes, corresponding to the gene complement found thus far in other flatworm mitochondrial (mt) DNAs. The gene arrangement of this pseudophyllidean cestode is the same as the 6 cyclophyllidean cestodes characterized to date, with only minor variation in structure among these other genomes; the relative position of trnS2 and trnL1 is switched in Hymenolepis diminuta. Phylogenetic analyses of the concatenated amino acid sequences for 12 protein-coding genes of all complete cestode mtDNAs confirmed taxonomic and previous phylogenetic assessments, with D. latum being a sister taxon to the cyclophyllideans. High nodal support and phylogenetic congruence between different methods suggest that mt genomes may be of utility in resolving ordinal relationships within the cestodes. All species of Diphyllobothrium infect fish-eating vertebrates, and D. latum commonly infects humans through the ingestion of raw, poorly cooked or pickled fish. The complete mitochondrial genome provides a wealth of genetic markers which could be useful for identifying different life-cycle stages and for investigating their population genetics, ecology and epidemiology.

Keywords

Diphyllobothrium latumdiphyllobothriasisPseudophyllideaCestodamitochondrial genomemolecular phylogeny
Type
Research Article
Information
Parasitology , Volume 134 , Issue 5 , May 2006 , pp. 749 - 759
Copyright
Copyright © Cambridge University Press 2007

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References

Adachi, J. and Hasegawa, M. (1996). Model of amino acid substitution in proteins encoded by mitochondrial DNA. Journal of Molecular Evolution 42, 459–468. doi: 10.1007/PL00013324CrossRefGoogle ScholarPubMed
Anderson, K. I. and Gibson, D. I. (1989). A key to 3 species of larval Diphyllobothrium Cobbold, 1858 (Cestoda, Pseudophyllidea) occurring in European and North-American freshwater fishes. Systematic Parasitology 13, 3–9.CrossRefGoogle Scholar
Ashford, R. W. and Crewe, W. (2003). The Parasites of Homo sapiens – an Annotaed Checklist of the Protozoa, Helminths and Arthropods for which we are Home, 2nd Edn. Taylor and Francis, London.Google Scholar
Avise, J. C. (2000). Phylogeography: The History and Formation of Species. Harvard University Press. Cambridge, Massachusetts.CrossRefGoogle Scholar
Boore, J. L. (1999). Animal mitochondrial genomes. Nucleic Acids Research 27, 1767–1780.CrossRefGoogle ScholarPubMed
Boore, J. L. and Brown, W. M. (2000). Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequences and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Molecular Biology and Evolution 17, 87–106.CrossRefGoogle Scholar
Brabec, J., Kuchta, R. and Scholz, T. (2006). Paraphyly of the Pseudophyllidea (Platyhelminthes: Cestoda): circumscription of monophyletic clades based on phylogenetic analysis of ribosomal RNA. International Journal for Parasitology 36, 1535–1541.CrossRefGoogle ScholarPubMed
Brooks, D. R., Hoberg, E. P. and Weekes, P. J. (1991). Preliminary phylogenetic systematic analysis of the major lineages of the Eucestoda (Platyhelminthes: Cercomeria). Proceedings of the Biological Society of Washington 104, 651–668.Google Scholar
Brown, W. M., Prager, E. M., Wang, A. and Wilson, A. C. (1982). Mitochondrial DNA sequences of primates: tempo and mode of evolution. Journal of Molecular Evolution 18, 225–239.CrossRefGoogle ScholarPubMed
Caira, J. N. and Littlewood, D. T. J. (2001). Diversity of Platyhelminthes. In Encyclopedia of Biodiversity, Vol. 5 (ed. Levin, S. A.), pp. 863–899. Academic Press, New York.CrossRefGoogle Scholar
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.CrossRefGoogle ScholarPubMed
Ehlers, U. (1985). Das phylogenetische System der Platyhelminthes. Gustav Fischer, Stuttgart.Google Scholar
Hardman, M. and Hardman, L. M. (2006). Comparison of the phylogenetic performance of neodermatan mitochondrial protein-coding genes. Zoologica Scripta 35, 655–665.CrossRefGoogle Scholar
Herbeck, J. T. and Novembre, J. (2003). Codon usage patterns in cytochrome oxidase I across multiple insect orders. Journal of Molecular Evolution 56, 691–701. doi: 10.1007/s00239-002-2437-7CrossRefGoogle ScholarPubMed
Hoberg, E. P., Mariaux, J., Justine, J.-L., Brooks, D. R. and Weekes, P. J. (1997). Phylogeny of the orders of the Eucestoda (Cercomeromorphae) based on comparative morphology: historical perspectives and a new working hypothesis. Journal of Parasitology 83, 1128–1147.CrossRefGoogle Scholar
Hoberg, E. P., Gardner, S. L. and Campbell, R. A. (1999). Systematics of the Eucestoda: advances toward a new phylogenetic paradigm, and observation on the early diversification of tapeworms and vertebrates. Systematic Parasitology 42, 1–12.CrossRefGoogle Scholar
Hoberg, E. P., Mariaux, J. and Brooks, D. R. (2001). Phylogeny among orders of the Eucestoda (Cercomeromorphae): integrating morphology, molecules and total evidence. In Interrelationships of the Platyhelminthes (ed. Littlewood, D. T. J. and Bray, R. A.), pp. 112–126. Taylor and Francis, London.Google Scholar
Hu, M., Chilton, N. B. and Gasser, R. B. (2004). The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress, and implications for population genetics and systematics. Advances in Parasitology 56, 133–212.CrossRefGoogle ScholarPubMed
Hu, M. and Gasser, R. B. (2006). Mitochondrial genomes of parasitic nematodes – progress and perspectives. Trends in Parasitology 22, 78–84. doi: 10.1016/j.pt.2005.12.003CrossRefGoogle Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755. doi: 10.1093/bioinformatics/17.8.754CrossRefGoogle Scholar
Jeon, H. K., Lee, K. H., Kim, K. H., Hwang, U. W. and Eom, K. S. (2005). Complete sequence and structure of the mitochondrial genome of the human tapeworm, Taenia asiatica (Platyhelminthes; Cestoda). Parasitology 130, 717–726. doi: 10.1017/S0031182004007164CrossRefGoogle ScholarPubMed
Johnston, D. A. (2006). Genomes and genomics of parasitic flatworms. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 37–80. CAB International, Wallingford, Oxford.CrossRefGoogle Scholar
Kim, K.-H., Eom, K. S. and Park, J.-K. (2006). The complete mitochondrial genome of Anisakis simplex (Ascaridida: Nematoda) and phylogenetic implications. International Journal for Parasitology 36, 319–328. doi: 10.1016/j.ijpara.2005.10.004CrossRefGoogle ScholarPubMed
Lavrov, D. V., Brown, W. M. and Boore, J. L. (2004). Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proceedings of the Royal Society of London, B 271, 537–544. doi: 10.1098/rspb.2003.2631CrossRefGoogle ScholarPubMed
Lavrov, D. V. and Lang, B. F. (2005). Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. Systematic Biology 54, 651–659. doi: 10.1080/10635150500221044CrossRefGoogle ScholarPubMed
Le, T. H., Blair, D., Agatsuma, T., Humair, P.-F., Campbell, N. J. H., Iwagami, M., Littlewood, D. T. J., 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 Scholar
Le, T. H., Humair, P.-F., Blair, D., Agatsuma, T., Littlewood, D. T. J. and McManus, D. P. (2001). Mitochondrial gene content, arrangement and composition compared in African and Asian schistosomes. Molecular and Biochemical Parasitology 117, 61–71. doi: 10.1016/S0166-6851(01)00330-9CrossRefGoogle ScholarPubMed
Le, T. H., Blair, D. and McManus, D. P. (2002 a). Mitochondrial genomes of parasitic flateworms. Trends in Parasitology 18, 206–213. doi: 10.1016/S1471-4922(02)02252-3CrossRefGoogle Scholar
Le, T. H., Pearson, M. S., Blair, D., Dai, N., Zhang, L. H. and McManus, D. P. (2002 b). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97–112. doi: 10.1017/S0031182001008976CrossRefGoogle ScholarPubMed
Le, T. H., van De, N., Blair, D., Sithithaworn, P. and McManus, D. P. (2006). Clonorchis sinensis and Opisthorchis viverrini: development of a mitochondrial-based multiplex PCR for their identification and discrimination. Experimental Parasitology 112, 109–114. doi: 10.1016/j.exppara.2005.09.012CrossRefGoogle Scholar
Lee, S.-H., Chai, J.-Y., Hong, S.-T., Sohn, W.-M., Huh, S., Cheong, E.-H. and Kang, S.-B. (1989). Seven cases of Diphyllobothrium latum infection. Korean Journal of Parasitology 27, 213–216.CrossRefGoogle ScholarPubMed
Littlewood, D. T. J., Cribb, T. H., Olson, P. D. and Bray, R. A. (2001). Platyhelminth phylogenetics – a key to understanding parasitism? Belgian Journal of Zoology 131 (Suppl. 1), 35–46.Google Scholar
Littlewood, D. T. J., Lockyer, A. E., Webster, B. L., Johnston, D. A. and Le, T. H. (2006). The complete mitochondrial genomes of Schistosoma haematobium and Schistosoma spindale and the evolutionary history of mitochondrial genome changes among parasitic flatworms. Molecular Phylogenetics and Evolution 39, 452–467. doi: 10.1016/j.ympev.2005.12.012CrossRefGoogle ScholarPubMed
Macpherson, C. N. L. (2005). Human behaviour and the epidemiology of parasitic zoonoses. International Journal for Parasitology 35, 1319–1331. doi: 10.1016/j.ijpara.2005.06.004CrossRefGoogle ScholarPubMed
Mariaux, J. (1996). Cestode systematics: Any progress? International Journal for Parasitology 26, 231–243. doi: 10.1016/0020-7519(95)00129-8CrossRefGoogle ScholarPubMed
Mariaux, J. (1998). A molecular phylogeny of the Eucestoda. Journal of Parasitology 84, 114–124.CrossRefGoogle ScholarPubMed
Matzura, O. and Wennborg, A. (1996). RNAdraw: an integrated program for RNA secondary structure calculation and analysis under 32-bit Microsoft Windows. Computer Applications in the Biosciences 12, 247–249.Google ScholarPubMed
McManus, D. P. (2006). Genetic discrimination of Echinococcus species and strains. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 81–95. CAB International, Wallingford, Oxford.CrossRefGoogle Scholar
Miyadera, H., Kokaze, A., Kuramochi, T., Kita, K., Machinami, R., Noya, O., de Noya, B. A., Okamoto, M. and Kojima, S. (2001). Phylogenetic identification of Sparganum proliferum as a pseudophyllidean cestode by the sequence analyses on mitochondrial COI and nuclear sdhB genes. Parasitology International 50, 93–104. doi: 10.1016/S1383-5769(01)00071-XCrossRefGoogle ScholarPubMed
Nakao, M., Yokoyama, N., Sako, Y., Fukunaga, M. and Ito, A. (2002). The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 1, 497–509. doi: 10.1016/S1567-7249(02)00040-5CrossRefGoogle ScholarPubMed
Nakao, M., Sako, Y. and Ito, A. (2003). The mitochondrial genome of the tape worm Taenia solium: a finding of the abbreviated stop codon U. Journal of Parasitology 89, 633–635. doi: 10.1645/0022-3395(2003)089[0633:TMGOTT]2.0.CO;2CrossRefGoogle Scholar
Olson, D. P., Littlewood, D. T. J., Bray, R. A. and Mariaux, J. (2001). Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 19, 443–467. doi: 10.1006/mpev.2001.0930CrossRefGoogle ScholarPubMed
Park, J.-K., Kim, K.-H., Kang, S., Kim, W., Eom, K. S. and Littlewood, D. T. J. (2007). A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of Microcotyle sebastis (Monogenea: Platyhelminthes). BMC Evolutionary Biology 7:11. doi: 10.1186/1471-2148-7-11CrossRefGoogle ScholarPubMed
Peduzzi, R. and Boucher-Rodoni, R. (2004). Resurgence of human bothriocephalosis (Diphyllobothrium latum) in the subalpine lake region. Journal of Limnology 60, 41–44.Google Scholar
Rausch, R. L. and Hilliard, D. K. (1970). Studies on the helminth fauna of Alaska. XLIX. The occurrence of Diphyllobothrium latum (Linnaeus, 1758) (Cestoda: Diphyllobothriidae) in Alaska, with notes on the species. Canadian Journal of Zoology 48, 1201–1219.CrossRefGoogle Scholar
Saccone, C., Gissi, C., Reyes, A., Larizza, A., Sbisà, E. and Pesole, G. (2002). Mitochodrial DNA in metazoa: degree of freedom in a frozen event. Gene 286, 3–12.CrossRefGoogle Scholar
Sampaio, J. L., de Andrade, V. P., Lucas Mda, C., Fung, L., Gagliardi, S. M., Santos, S. R., Mendes, C. M., Eduardo, M. B. and Dick, T. (2005). Diphyllobothriasis, Brazil. Emerging Infectious Diseases 11, 1598–1600.CrossRefGoogle ScholarPubMed
Santos, F. L. N. and de Faro, L. B. (2005). The first confirmed case of Diphyllobothrium latum in Brazil. Memórias do Instituto Oswaldo Cruz 100, 585–586. doi: 10.1590/S0074-02762005000600013CrossRefGoogle ScholarPubMed
Schmidt, H. A., Strimmer, K., Vingron, M. and von Haeseler, A. (2002). TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504. doi: 10.1093/bioinformatics/18.3.502CrossRefGoogle ScholarPubMed
Scouras, A. and Smith, M. J. (2001). A novel mitochondrial gene order in the crinoid echinoderm Florometra serratissima. Molecular Biology and Evolution 18, 61–73.CrossRefGoogle ScholarPubMed
Skerikova, A., Brabec, J., Kuchta, R., Jimenez, J. A., Garcia, H. H. and Scholz, T. (2006). Is the human-infecting Diphyllobothrium pacificum a valid species or just a South American population of the holarctic fish broad tapeworm, D. latum? The American Journal of Tropical Medicine and Hygiene 75, 307–310.CrossRefGoogle ScholarPubMed
Strimmer, K. and von Haeseler, A. (1997). Likelihood mapping: a simple method to visualize phylogenetic content in a sequence alignment. Proceedings of the National Academy of Sciences, USA 94, 6815–6819.CrossRefGoogle Scholar
Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (*and other Methods) Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882. doi: 10.1093/nar/25.24.4876CrossRefGoogle Scholar
von Nickisch-Rosenegk, M., Brown, W. M. and Boore, J. L. (2001). Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that platyhelminths are Eutrochozoans. Molecular Biology and Evolution 18, 721–830.CrossRefGoogle ScholarPubMed
Yamane, Y., Shiwaku, K., Fukushima, T., Isobe, A., Yoneyama, T., Qiang, G. T. and Jie, W. C. (1996). The recent situation of diphyllobothriasis in Japan: epidemiology, taxonomy and clinical features. Proceedings of the 2nd Japan-Korea Parasitologists. Seminar (Forum Cheju-2), pp. 74–78.Google Scholar
Yera, H., Estran, C., Delaunay, P., Gari-Toussaint, M., Dupouy-Camet, J. and Marty, P. (2006). Putative Diphyllobothrium nihonkaiense acquired from a Pacific salmon (Oncorhynchus keta) eaten in France; genomic identification and case report. Parasitology International 55, 45–49. doi: 10.1016/j.parint.2005.09.004CrossRefGoogle ScholarPubMed
Wyman, S. K., Jansen, R. K. and Boore, J. L. (2004). Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20, 3252–3255. doi: 10.1093/bioinformatics/bth352CrossRefGoogle ScholarPubMed