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Sequence variability in two mitochondrial DNA regions and internal transcribed spacer among three cestodes infecting animals and humans from China

Published online by Cambridge University Press:  12 July 2011

R.S. Dai
Affiliation:
College of Veterinary Medicine, Hunan Agricultural University, Changsha, Hunan Province410128, PR China State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, Gansu Province730046, PR China
G.H. Liu
Affiliation:
College of Veterinary Medicine, Hunan Agricultural University, Changsha, Hunan Province410128, PR China State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, Gansu Province730046, PR China
H.Q. Song
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, Gansu Province730046, PR China College of Veterinary Medicine, South China Agricultural University, Guangzhou, Guangdong Province510642, PR China
R.Q. Lin
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, Gansu Province730046, PR China College of Veterinary Medicine, South China Agricultural University, Guangzhou, Guangdong Province510642, PR China
Z.G. Yuan
Affiliation:
College of Veterinary Medicine, South China Agricultural University, Guangzhou, Guangdong Province510642, PR China
M.W. Li
Affiliation:
Department of Veterinary Medicine, Guangdong Ocean University, Zhanjiang, Guangdong Province524088, PR China
S.Y. Huang
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, Gansu Province730046, PR China
W. Liu*
Affiliation:
College of Veterinary Medicine, Hunan Agricultural University, Changsha, Hunan Province410128, PR China State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, Gansu Province730046, PR China
X.Q. Zhu*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, Gansu Province730046, PR China College of Animal Science and Technology, Yunnan Agricultural University, Kunming, Yunnan Province650201, PR China
*
*Fax: +86 (931) 8340977 E-mail: xingquanzhu1@hotmail.com (X.Q.Z.); E-mail: liuwpro@163.com (W.L.)
*Fax: +86 (931) 8340977 E-mail: xingquanzhu1@hotmail.com (X.Q.Z.); E-mail: liuwpro@163.com (W.L.)

Abstract

Sequence variability in two mitochondrial DNA (mtDNA) regions, namely cytochrome c oxidase subunit 1 (cox1) and NADH dehydrogenase subunit 4 (nad4), and internal transcribed spacer (ITS) of rDNA among and within three cestodes, Spirometra erinaceieuropaei, Taenia multiceps and Taenia hydatigena, from different geographical origins in China was examined. A portion of the cox1 (pcox1), nad4 genes (pnad4) and the ITS (ITS1+5.8S rDNA+ITS2) were amplified separately from individual cestodes by polymerase chain reaction (PCR). Representative amplicons were subjected to sequencing in order to estimate sequence variability. While the intra-specific sequence variations within each of the tapeworm species were 0–0.7% for pcox1, 0–1.7% for pnad4 and 0.1–3.6% for ITS, the inter-specific sequence differences were significantly higher, being 12.1–17.6%, 18.7–26.2% and 31–75.5% for pcox1, pnad4 and ITS, respectively. Phylogenetic analyses based on the pcox1 sequence data revealed that T. multiceps and T. hydatigena were more closely related to the other members of the Taenia genus, and S. erinaceieuropaei was more closely related to the other members of the Spirometra genus. These findings demonstrated clearly the usefulness of mtDNA and rDNA sequences for population genetic studies of these cestodes of socio-economic importance.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2011

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References

Agatsuma, T., Iwagami, M., Sato, Y., Iwashita, J., Hong, S.J., Kang, S.Y., Ho, L.Y., Su, K.E., Kawashima, K. & Abe, T. (2003) The origin of the triploid in Paragonimus westermani on the basis of variable regions in the mitochondrial DNA. Journal of Helminthology 77, 279285.CrossRefGoogle ScholarPubMed
Benifla, M., Barrelly, R., Shelef, I., El-On, J., Cohen, A. & Cagnano, E. (2007) Huge hemispheric intraparenchymal cyst caused by Taenia multiceps in a child. Case report. Journal of Neurosurgery 107, 511514.Google Scholar
Bowles, J. & McManus, D.P. (1994) Genetic characterization of the Asian Taenia, a newly described taeniid cestode of humans. American Journal of Tropical Medicine and Hygiene 50, 3344.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. & McManus, D.P. (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.CrossRefGoogle ScholarPubMed
Chapman, A., Vallejo, V., Mossie, K.G., Ortiz, D., Agabian, N. & Flisser, A. (1995) Isolation and characterization of species-specific DNA probes from Taenia solium and Taenia saginata and their use in an egg detection assay. Journal of Clinical Microbiology 33, 12831288.Google Scholar
Chilton, N.B., Gasser, R.B. & Beveridge, I. (1995) Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology 25, 647651.Google Scholar
Collomb, J, Machouart, M., Biava, M.F., Brizion, M., Montagne, K., Plénat, F. & Fortier, B. (2007) Contribution of NADH dehydrogenase subunit I and cytochrome C oxidase subunit I sequences toward identifying a case of human coenuriasis in France. Journal of Parasitology 93, 934937.CrossRefGoogle ScholarPubMed
Dai, R.S., Li, Z.Y., Li, F., Liu, D.X., Liu, W., Liu, G.H., He, S.W., Tan, M.Y., Lin, R.Q., Liu, Y. & Zhu, X.Q. (2009) Severe infection of adult dogs with helminths in Hunan Province, China poses significant public health concerns. Veterinary Parasitology 160, 348350.CrossRefGoogle ScholarPubMed
Dalimi, A., Sattari, A. & Motamedi, G. (2006) A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Veterinary Parasitology 142, 129133.Google Scholar
Escobedo, G., Romano, M.C. & Montor, J.M. (2009) Differential in vitro effects of insulin on Taenia crassiceps and Taenia solium cysticerci. Journal of Helminthology 83, 403412.Google Scholar
Felsenstein, J. (1995) PHYLIP (Phylogeny Inference Package), version 3.57c, Department of Genetics, University of Washington, Seattle.Google Scholar
Foronda, P., Casanova, J.C., Martinez, E., Valladares, B. & Feliu, C. (2005) Taenia spp.: 18S rDNA microsatellites for molecular systematic diagnosis. Journal of Helminthology 79, 139142.Google Scholar
Gasser, R.B. & Chilton, N.B. (1995) Characterisation of taeniid cestode species by PCR-RFLP of ITS2 ribosomal DNA. Acta Tropica 59, 3140.CrossRefGoogle ScholarPubMed
Gasser, R.B., Zhu, X.Q. & McManus, D.P. (1999) NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda). International Journal for Parasitology 29, 19651970.Google Scholar
Gauci, C., Vural, G., Oncel, T., Varcasia, A., Damian, V., Kyngdon, C.T., Craig, P.S., Anderson, G.A. & Lightowlers, M.W. (2008) Vaccination with recombinant oncosphere antigens reduces the susceptibility of sheep to infection with Taenia multiceps. International Journal for Parasitology 38, 10411050.Google Scholar
González, L.M., Villalobos, N., Montero, E., Morales, J., Sanz, R.A., Muro, A., Harrison, L.J.S., Parkhouse, R.M.E. & Gárate, T. (2006) Differential molecular identification of Taeniid spp. and Sarcocystis spp. cysts isolated from infected pigs and cattle. Veterinary Parasitology 142, 95101.Google Scholar
Kralova, I., Hanzelova, V., Scholz, T., Gerdeaux, D. & Spakulova, M. (2001) A comparison of the internal transcribed spacer of the ribosomal DNA for Eubothrium crassum and Eubothrium salvelini (Cestoda: Pseudophyllidea), parasites of salmonid fish. International Journal for Parasitology 31, 9396.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. & McManus, D.P. (2000) Phylogenies inferred from mitochondrial gene orders – a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 11231125.Google Scholar
Le, T.H., Blair, D. & McManus, D.P. (2002) Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206213.CrossRefGoogle ScholarPubMed
Li, M.W., Lin, R.Q., Song, H.Q., Sani, R.A., Wu, X.Y. & Zhu, X.Q. (2008) Electrophoretic analysis of sequence variability in three mitochondrial DNA regions for ascaridoid parasites of human and animal health significance. Electrophoresis 29, 29122917.CrossRefGoogle ScholarPubMed
Luo, H.Y., Nie, P., Zhang, Y.A., Wang, G.T. & Yao, W.J. (2002) Molecular variation of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Pseudophyllidea) in different fish host species based on ITS rDNA sequences. Systematic Parasitology 52, 159166.CrossRefGoogle ScholarPubMed
Mayta, H., Talley, A., Gilman, R.H., Jimenez, J., Verastegui, M., Ruiz, M., Garcia, H.H. & Gonzalez, A.E. (2000) Differentiating Taenia solium and Taenia saginata infections by simple hematoxylin–eosin staining and PCR–restriction enzyme analysis. Journal of Clinical Microbiology 38, 133137.Google Scholar
Nakao, M., Sako, Y., Yokoyama, N., Fukunaga, M. & Ito, A.. (2000) Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415424.Google Scholar
Nakao, M., Okamoto, M., Sako, Y., Yamasaki, H., Nakaya, K. & Ito, A. (2002a) A phylogenetic hypothesis for the distribution of two genotypes of the pig tapeworm Taenia solium worldwide. Parasitology 124, 657662.CrossRefGoogle ScholarPubMed
Nakao, M., Yokoyama, N., Sako, Y., Fukunaga, M. & Ito, A. (2002b) The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 1, 497509.Google Scholar
Nakao, M., Abmed, D., Yamasaki, H.. & Ito, A.. (2007) Mitochondrial genomes of the human broad tapeworms Diphyllobothrium latum and Diphyllobothrium nihonkaiense (Cestoda: Diphyllobothriidae). Parasitology Research 101, 233236.Google Scholar
Nejad, M.R., Mojarad, E.N., Nochi, Z., Harandi, M.F., Cheraghipour, K., Mowlavi, G.R. & Zali, M.R. (2008) Echinococcus granulosus strain differentiation in Iran based on sequence heterogeneity in the mitochondrial 12S rRNA gene. Journal of Helminthology 82, 343347.CrossRefGoogle Scholar
Ngowi, H.A., Kassuku, A.A., Maeda, G.E., Boa, M.E. & Willingham, A.L. (2004) A slaughter slab survey for extra-intestinal porcine helminth infections in Northern Tanzania. Tropical Animal Health and Production 36, 335340.Google Scholar
Okamoto, M., Bessho, Y., Kamiya, M., Kurosawa, T. & Horii, T. (1995) Phylogenetic relationships within Taenia taeniaeformis variants and other taeniid cestodes inferred from the nucleotide sequence of the cytochrome c oxidase subunit I gene. Parasitology Research 81, 451458.CrossRefGoogle ScholarPubMed
Okamoto, M., Iseto, C., Shibahara, T., Sato, M.O., Wandra, T., Craig, P.S. & Ito, A. (2007) Intraspecific variation of Spirometra erinaceieuropaei and phylogenetic relationship between Spirometra and Diphyllobothrium inferred from mitochondrial CO1 gene sequences. Parasitology International 56, 235238.CrossRefGoogle ScholarPubMed
Page, R.D. (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357358.Google Scholar
Raccurt, C.P., Agnamey, P., Boncy, J., Henrys, J.H. & Totet, A. (2009) Seroprevalence of human Taenia solium cysticercosis in Haiti. Journal of Helminthology 83, 113116.Google Scholar
Sissay, M.M., Uggla, A. & Waller, P.J. (2008) Prevalence and seasonal incidence of larval and adult cestode infections of sheep and goats in eastern Ethiopia. Tropical Animal Health and Production 40, 387394.CrossRefGoogle ScholarPubMed
Strimmer, K. & Haeseler, A.V. (1996) Quartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13, 964969.CrossRefGoogle Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 48764882.Google Scholar
van Herwerden, L., Gasser, R.B. & Blair, D. (2000) ITS-1 ribosomal DNA sequence variants are maintained in different species and strains of Echinococcus. International Journal for Parasitology 30, 157169.CrossRefGoogle ScholarPubMed
Varcasia, A., Lightowlers, M.W., Cattoli, G., Cancedda, G.M., Canu, S., Garippa, G. & Scala, A. (2006) Genetic variation within Taenia multiceps in Sardinia, Western Mediterranean (Italy). Parasitology Research 99, 622626.Google Scholar
Yamasaki, H., Allan, J.C., Sato, M.O., Nakao, M., Sako, Y., Nakaya, K., Qiu, D., Mamuti, W., Craig, P.S. & Ito, A. (2004) DNA differential diagnosis of taeniasis and cysticercosis by multiplex PCR. Journal of Clinical Microbiology 42, 548553.CrossRefGoogle ScholarPubMed
Yang, Y.R., Rosenzvit, M.C., Zhang, L.H., Zhang, J.Z. & McManus, D.P. (2005) Molecular study of Echinococcus in west-central China. Parasitology 131, 547555.Google Scholar
Wang, C.R., Qiu, J.H., Zhao, J.P., Xu, L.M., Yu, W.C. & Zhu, X.Q. (2006) Prevalence of helminthes in adult dogs in Heilongjiang Province, the People's Republic of China. Parasitology Research 99, 627630.Google Scholar
Wickstro, L.M., Haukisalmi, V., Varis, S., Hantula, J. & Henttonen, H. (2005) Molecular phylogeny and systematics of anoplocephaline cestodes in rodents and lagomorphs. Systematic Parasitology 62, 8399.CrossRefGoogle Scholar
Zhang, L., Hu, M., Jones, A., Allsopp, B.A., Beveridge, I., Schindler, A.R. & Gasser, R.B. (2009) Characterization of Taenia madoquae and Taenia regis from carnivores in Kenya using genetic markers in nuclear and mitochondrial DNA, and their relationships with other selected taeniids. Molecular and Cellular Probes 21, 379385.Google Scholar
Zhao, G.H., Mo, X.H., Zou, F.C., Weng, Y.B., Lin, R.Q., Xia, C.M. & Zhu, X.Q. (2009) Genetic variability among Schistosoma japonicum isolates from different endemic regions in China revealed by sequences of three mitochondrial DNA genes. Veterinary Parasitology 162, 6774.CrossRefGoogle Scholar
Zhu, X.Q., Chilton, N.B., Jacobs, D.E., Boes, J. & Gasser, R.B. (1999) Characterisation of Ascaris from human and pig hosts by nuclear ribosomal DNA sequences. International Journal for Parasitology 29, 469478.Google Scholar