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The mitochondrial genome of Gyrodactylus salaris (Platyhelminthes: Monogenea), a pathogen of Atlantic salmon (Salmo salar)

Published online by Cambridge University Press:  11 December 2006

T. HUYSE ,
L. PLAISANCE ,
B. L. WEBSTER ,
T. A. MO ,
T. A. BAKKE ,
L. BACHMANN  and
D. T. J. LITTLEWOOD
T. HUYSE*
Affiliation:
Parasitic Worms Group, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
L. PLAISANCE
Affiliation:
The Natural History Museum, Department of Zoology, University of Oslo, P.O. Box 1172, Blindern, NO-0318 Oslo, Norway Marine Biology Research Division 0202, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, CA 92093-0202, USA
B. L. WEBSTER
Affiliation:
Parasitic Worms Group, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
T. A. MO
Affiliation:
National Veterinary Institute, P.O. Box 8156 Dep., NO-0033 Oslo 1, Norway
T. A. BAKKE
Affiliation:
The Natural History Museum, Department of Zoology, University of Oslo, P.O. Box 1172, Blindern, NO-0318 Oslo, Norway
L. BACHMANN
Affiliation:
The Natural History Museum, Department of Zoology, University of Oslo, P.O. Box 1172, Blindern, NO-0318 Oslo, Norway
D. T. J. LITTLEWOOD
Affiliation:
Parasitic Worms Group, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: Parasitic Worms Group, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK. Tel: +442079426115. Fax: +442079425151. E-mail: T.Huyse@nhm.ac.uk
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Summary

In the present study, we describe the complete mitochondrial (mt) genome of the Atlantic salmon parasite Gyrodactylus salaris, the first for any monogenean species. The circular genome is 14 790 bp in size. All of the 35 genes recognized from other flatworm mitochondrial genomes were identified, and they are transcribed from the same strand. The protein-coding and ribosomal RNA (rRNA) genes share the same gene arrangement as those published previously for neodermatan mt genomes (representing cestodes and digeneans only), and the genome has an overall A+T content of 65%. Three transfer RNA (tRNA) genes overlap with other genes, whereas the secondary structure of 3 tRNA genes lack the DHU arm and 1 tRNA gene lacks the TΨC arm. Eighteen regions of non-coding DNA ranging from 4 to 112 bp in length, totalling 278 bp, were identified as well as 2 large non-coding regions (799 bp and 768 bp) that were almost identical to each other. The completion of the mt genome offers the opportunity of defining new molecular markers for studying evolutionary relationships within and among gyrodactylid species.

Keywords

mitochondrial genomeGyrodactylus salarisMonopisthocotyleaSalmo salargyrodactylosis
Type
Research Article
Information
Parasitology , Volume 134 , Issue 5 , May 2006 , pp. 739 - 747
Copyright
Copyright © Cambridge University Press 2006

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References

REFERENCES

Bakke, T. A., Cable, J. and Harris, P. D. (2006). The biology of gyrodactylid monogeneans: the “Russian Doll-killers”. Advances in Parasitology (in the Press).Google Scholar
Bakke, T. A., Harris, P. D. and Cable, J. (2002). Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308.CrossRefGoogle ScholarPubMed
Benson, G. (1999). Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research 27, 573–580.CrossRefGoogle Scholar
Boore, J. L. and Brown, W. M. (2000). Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence 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
Boore, J. L., Macey, J. R. and Medina, M. (2005). Sequencing and comparing whole mitochondrial genomes of animals. Molecular Evolution: Producing the Biochemical Data, Part B 395, 311–348.Google ScholarPubMed
Cunningham, C. O. (1997). Species variation within the internal transcribed spacer (ITS) region of Gyrodactylus (Monogenea: Gyrodactylidae) ribosomal RNA genes. Journal of Parasitology 83, 215–219.CrossRefGoogle Scholar
Cunningham, C. O., Collins, C. M., Malmberg, G. and Mo, T. A. (2003). Analysis of ribosomal RNA intergenic spacer (IGS) sequences in species and populations of Gyrodactylus (Platyhelminthes: Monogenea) from salmonid fish in northern Europe. Diseases of Aquatic Organisms 57, 237–246.CrossRefGoogle ScholarPubMed
Després, L., Imbert-Establet, D., Combes, C., Bonhomme, F. and Monnerot, M. (1991). Isolation and polymorphism in mitochondrial DNA from Schistosoma mansoni. Molecular and Biochemical Parasitology 47, 139–142.CrossRefGoogle ScholarPubMed
Hansen, H., Bachmann, L. and Bakke, T. A. (2003). Mitochondrial DNA variation of Gyrodactylus spp. (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling, and rainbow trout in Norway and Sweden. International Journal for Parasitology 33, 1471–1478.CrossRefGoogle ScholarPubMed
Hansen, H., Martinsen, L., Bakke, T. A. and Bachmann, L. (2006). The incongruence of nuclear and mitochondrial DNA variation supports conspecificity of the monogenean parasites Gyrodactylus salaris and G. thymalli. Parasitology 133, 639–650.CrossRefGoogle ScholarPubMed
Harris, P. D., Shinn, A. P., Cable, J. and Bakke, T. A. (2004). Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Systematic Parasitology 59, 1–27.CrossRefGoogle ScholarPubMed
Huyse, T., Audenaert, V. and Volckaert, F. A. M. (2003). Speciation and host-parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). International Journal for Parasitology 33, 1679–1689.CrossRefGoogle ScholarPubMed
Johnsen, B. O., Møkkelgjerd, P. I. and Jensen, A. J. (1999). The parasite Gyrodactylus salaris on salmon parr in Norwegian rivers, status report at the beginning of year 2000. (In Norwegian, English summary). NINA Oppdargsmelding 617, 1–129.Google Scholar
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. CABI, Wallingford.CrossRefGoogle Scholar
Le, T. H., Blair, D. and McManus, D. P. (2002). Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206–213.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lowe, T. M. and Eddy, S. R. (1997). tRNAscan-SE: a program for improved transfer RNA detection in genomic sequence. Nucleic Acids Research 25, 955–964.CrossRefGoogle ScholarPubMed
Matejusová, I., Gelnar, M., Verneau, O., Cunningham, C. O. and Littlewood, D. T. J. (2003). Molecular phylogenetic analysis of the genus Gyrodactylus (Platyhelminthes: Monogenea) inferred from rDNA ITS region: subgenera versus species groups. Parasitology 127, 603–611.CrossRefGoogle ScholarPubMed
Meinila, M., Kuusela, J., Zietara, M. S. and Lumme, J. (2004). Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). International Journal for Parasitology 34, 515–526.CrossRefGoogle ScholarPubMed
Mo, T. A. (2006). Chapter 2.1.14. Gyrodactylosis (Gyrodactylus salaris) [online manual]. World Organization for Animal Health. http://www.oie.int/eng/normes/fmanual/A_00031.htmGoogle Scholar
Mo, T. A. and Norheim, K. (2005). The surveillance and control programme for Gyrodactylus salaris in Atlantic salmon and rainbow trout in Norway. In Annual Report 2004, pp. 137–139. National Veterinary Institute.Google Scholar
Mo, T. A., Norheim, K. and Hellesnes, I. (2004). The surveillance and control programme for Gyrodactylus salaris in Atlantic salmon and rainbow trout in Norway. (In Norwegian, English summary.) Norsk Veterinærtidsskrift 3, 157–163.Google Scholar
Olstad, K., Robertsen, G., Bachmann, L. and Bakke, T. A. (2006). Intraspecific differences in host preference among Gyrodactylus salaris (Monogenea) strains: an experimental approach. Parasitology (in the Press).Google Scholar
Peeler, E. J. and Thrush, M. A. (2004). Qualitative analysis of the risk of introducing Gyrodactylus salaris into the United Kingdom. Diseases of Aquatic Organisms 62, 103–113.CrossRefGoogle ScholarPubMed
Peeler, E. J., Thrush, M. A., Paisley, L. and Rodgers, C. (2006). An assessment of the risk of spreading the fish parasite Gyrodactylus salaris to uninfected territories in the European Union with the movement of live Atlantic salmon (Salmo salar) from coastal waters. Aquaculture 258, 187–197.CrossRefGoogle Scholar
Place, A. R., Feng, X. J., Steven, C. R., Fourcade, H. M. and Boore, J. L. (2005). Genetic markers in blue crabs (Callinectes sapidus) II. Complete mitochondrial genome sequence and characterization of genetic variation. Journal of Experimental Marine Biology and Ecology 319, 15–27.CrossRefGoogle Scholar
Poléo, A. B. S., Schjolden, J., Hansen, H., Bakke, T. A., Mo, T. A., Rosseland, B. O. and Lydersen, E. (2004). The effect of various metals on Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon (Salmo salar). Parasitology 128, 1–9.Google ScholarPubMed
Robertsen, G., Hansen, H., Bachmann, L. and Bakke, T. A. (2006). Arctic charr (Salvelinus alpinus) is a suitable host for Gyrodactylus salaris (Monogenea, Gyrodactylidae) in Norway. Parasitology (in the Press).Google ScholarPubMed
Shinn, A. P., Gibson, D. I. and Sommerville, C. (2001). Morphometric discrimination of Gyrodactylus salaris Malmberg (Monogenea) from species of Gyrodactylus parasitising British salmonids using novel parameters. Journal of Fish Diseases 24, 83–97.CrossRefGoogle Scholar
Shinn, A. P., Hansen, H., Olstad, K., Bachmann, L. and Bakke, T. A. (2004). The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitologica 51, 239–252.CrossRefGoogle Scholar
Soleng, A., Poleo, A. B. S., Alstad, N. E. W. and Bakke, T. A. (1999). Aqueous aluminium eliminates Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon. Parasitology 119, 19–25.CrossRefGoogle ScholarPubMed
Soleng, A., Poleo, A. B. S. and Bakke, T. A. (2005). Toxicity of aqueous aluminium to the ectoparasitic monogenean Gyrodactylus salaris. Aquaculture 250, 616–620.CrossRefGoogle Scholar
Sterud, E., Mo, T. A., Collins, C. M. and Cunningham, C. O. (2002). The use of host specificity, pathogenicity, and molecular markers to differentiate between Gyrodactylus salaris Malmberg, 1957 and G. thymalli Zitnan, 1960 (Monogenea: Gyrodactylidae). Parasitology 124, 203–213.CrossRefGoogle Scholar
Telford, M. J., Herniou, E. A., Russell, R. B. and Littlewood, D. T. J. (2000). Changes in mitochondrial genetic codes as phylogenetic characters: two examples from the flatworms. Proceedings of the National Academy of Sciences, USA 97, 11359–11364.CrossRefGoogle ScholarPubMed
Wolstenholme, D. R. (1992). Animal mitochondrial DNA: structure and evolution. International Reviews in Cytology 141, 173–216.CrossRefGoogle ScholarPubMed
Zietara, M. S., Huyse, T., Lumme, J. and Volckaert, F. A. (2002). Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 124, 39–52.CrossRefGoogle ScholarPubMed