Hostname: page-component-77c89778f8-gq7q9 Total loading time: 0 Render date: 2024-07-16T18:00:09.015Z Has data issue: false hasContentIssue false

First report of Echinococcus granulosus G8 in Eurasia and a reappraisal of the phylogenetic relationships of ‘genotypes’ G5-G10

Published online by Cambridge University Press:  11 February 2008

E. MOKS
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014 Tartu, Estonia
I. JÕGISALU
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014 Tartu, Estonia Centre of Forest Protection and Silviculture, Rõõmu tee 2, 51013 Tartu, Estonia
H. VALDMANN
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014 Tartu, Estonia
U. SAARMA*
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014 Tartu, Estonia Estonian Biocentre, Riia 23, 51010 Tartu, Estonia
*
*Corresponding author: Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia. Tel: +3727375099. Fax: +3727375830. E-mail: Urmas.Saarma@ut.ee

Summary

In this study, we investigated the presence of the larval stage of the tapeworm Echinococcus granulosus in wild ungulates in Estonia, genetically characterized E. granulosus isolates using mitochondrial gene sequences and used the sequence data, together with those available in a public database, to infer the phylogenic relationships of E. granulosus ‘genotypes’ G5-G10. While 0·8% of the 2038 moose (Alces alces) examined were found to be infected with E. granulosus, the parasite was not detected in other wild ungulates, such as roe deer (Capreolus capreolus: 1044 specimens examined) and wild boar (Sus scrofa: 442 specimens). Genetic analyses of concatenated atp6, nad1 and cox1 gene (1028 bp) sequences revealed that 2 novel E. granulosus haplotypes, namely E8 (11 samples: 69%) and E10 (5 samples: 31%), grouped with E. granulosus G8 and G10, respectively, are present in Estonia. This is the first record of an E. granulosus G8 in Eurasia. Phylogenetic analyses, using 4 different methods, demonstrated with considerable statistical support that E. granulosus G6/7 forms a subgroup together with G10, whereas G8 is a sister taxon to G6/7-G10.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abuladze, K. I. (1964). Echinococcus granulosus (Batsch, 1786) Rudolphi 1801. In Principles of Cestodology Vol. IV. Taeniidae – Cestodes of Animals and Man and the Diseases they Provoke (ed. Skrjabin, K. I.). pp. 314339. Nauka, Moscow (in Russian).Google Scholar
Bandelt, H.-J., Forster, P. and Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.CrossRefGoogle ScholarPubMed
Beveridge, I., Shamsi, S., Hu, M., Chilton, N. B, and Gasser, R. B. (2007). Genetic variation in the mitochondrial cytochrome c oxidase subunit 1 within Progamotaenia festiva (Cestoda: Anoplocephalidae) from macropodid marsupials. Parasitology 134, 14651476.Google Scholar
Bhattacharya, D., Bera, A. K., Bera, B. C., Maity, A. and Das, S. K. (2007). Genotypic characterisation of Indian cattle, buffalo and sheep isolates of Echinococcus granulosus. Veterinary Parasitology 143, 371374.Google Scholar
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.Google Scholar
Bowles, J., Blair, D. and McManus, D. P. (1994). Molecular genetic characterization of the cervid strain (‘northern form’) of Echinococcus granulosus. Parasitology 109, 215221.CrossRefGoogle ScholarPubMed
Bowles, J. and McManus, D. P. (1993). NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. International Journal for Parasitology 23, 969972.Google Scholar
Gordon, D., Abajian, C. and Green, P. (1998). Consed: A graphical tool for sequence finishing. Genome Research 8, 195202.Google Scholar
Hall, T. A. (1999). BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41, 9598.Google Scholar
Hirvelä-Koski, V., Haukisalmi, V., Kilpelä, S.-S., Nylund, M. and Koski, P. (2003). Echinococcus granulosus in Finland. Veterinary Parasitology 111, 175192.Google Scholar
Itagaki, T., Kikawa, M., Sakaguchi, K., Shimo, J., Terasaki, K., Shibahara, T. and Fukuda, K. (2005). Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology 131, 679685.Google Scholar
Järvis, T. (1993). Helminth fauna of wild ungulates in Estonia and control of helminthoses. Ph.D. dissertation/ Estonian University of Agricultural Sciences, Tartu (in Estonian).Google Scholar
Kedra, A. H., Swiderski, Z., Tkach, V. V., Dubinsky, P., Pawlowski, Z., Stefaniak, J. and Pawlowski, J. (1999). Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia and Ukraine. A multicenter study. Acta Parasitologica 44, 248254.Google Scholar
Lavikainen, A., Lehtinen, M. J., Laaksonen, S., Ågren, E., Oksanen, A. and Meri, S. (2006). Molecular characterization of Echinococcus isolates of cervid origin from Finland and Sweden. Parasitology 133, 565570.Google Scholar
Lavikainen, A., Lehtinen, M. J., Meri, T., Hirvelä-Koski, V. and Meri, S. (2003). Molecular genetic characterization of the Fennoscandian cervid strain, a new genotype group (G10) of Echinococcus granulosus. Parasitology 127, 207215.Google Scholar
Le, T. H., Pearson, M. S., Blair, D., Dai, N., Zhang, L. H. and McManus, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97112.Google Scholar
Lesinš, K. L. (1955). Analysis of Helminth Fauna and Seasonal Dynamics of Helminthosis of Farm Animals in South-East of ESSR. Candidate Dissertation, Tartu – Moscow(in Russian).Google Scholar
Moks, E., Jõgisalu, I., Saarma, U., Talvik, H., Järvis, T. and Valdmann, H. (2006). Helminthologic survey of the wolf (Canis lupus) in Estonia, with an emphasis on Echinococcus granulosus. Journal of Wildlife Diseases 42, 359365.Google Scholar
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713722.Google Scholar
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, 497509.Google Scholar
Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357358.Google ScholarPubMed
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818.Google Scholar
Rausch, R. L. (1967). On the ecology and distribution of Echinococcus spp. (Cestoda:Taeniidae), and characteristics of their development in the intermediate host. Annales de Parasitologie Humaine et Comparée (Paris) 42, 1963.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.Google Scholar
Scott, J. C., Stefaniak, J., Pawlowski, Z. S. and McManus, D. P. (1997). Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114, 3743.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2003). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts, USA.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.Google Scholar
Thompson, R. C. A. and McManus, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452457.Google Scholar
Thompson, R. C. A., Boxell, A. C., Ralston, B. J., Constantine, C. C., Hobbs, R. P., Shury, T. and Olson, M. E. (2006). Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology 132, 439447.CrossRefGoogle ScholarPubMed
Thompson, R. C. A., Lymbery, A. J. and Constantine, C. C. (1995). Variation in Echinococcus: towards a taxonomic revision of the genus. Advances in Parasitology 35, 145176.Google Scholar
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. (2005). Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693701.Google Scholar