Hostname: page-component-7c8c6479df-xxrs7 Total loading time: 0 Render date: 2024-03-28T14:46:48.377Z Has data issue: false hasContentIssue false

Microdiversity of Echinococcus granulosus sensu stricto in Australia

Published online by Cambridge University Press:  04 April 2016

C. A. ALVAREZ ROJAS*
Affiliation:
Faculty of Veterinary and Agricultural Sciences, Centre for Animal Biotechnology, The University of Melbourne, Parkville, Victoria 3010, Australia
D. EBI
Affiliation:
Parasitology Unit, University of Hohenheim, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
C. G. Gauci
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
J. P. SCHEERLINCK
Affiliation:
Faculty of Veterinary and Agricultural Sciences, Centre for Animal Biotechnology, The University of Melbourne, Parkville, Victoria 3010, Australia
M. WASSERMANN
Affiliation:
Parasitology Unit, University of Hohenheim, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
D. J. JENKINS
Affiliation:
School of Animal and Veterinary Sciences, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia
M. W. LIGHTOWLERS
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
T. ROMIG
Affiliation:
Parasitology Unit, University of Hohenheim, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
*
*Corresponding author: Faculty of Veterinary and Agricultural Sciences, Centre for Animal Biotechnology, The University of Melbourne, Parkville, Victoria 3010, Australia. E-mail: alvarezc@unimelb.edu.au

Summary

Echinococcus granulosus (sensu lato) is now recognized as an assemblage of cryptic species, which differ considerably in morphology, development, host specificity (including infectivity/pathogenicity for humans) and other aspects. One of these species, E. granulosus sensu stricto (s.s.), is now clearly identified as the principal agent causing cystic echinococcosis in humans. Previous studies of a small section of the cox1 and nadh1 genes identified two variants of E. granulosus s.s. to be present in Australia; however, no further work has been carried out to characterize the microdiversity of the parasite in its territory. We have analysed the sequence of the full length of the cox1 gene (1609 bp) from 37 isolates of E. granulosus from different hosts and geographic regions of Australia. The analysis shows that seven haplotypes of E. granulosus s.s. not previously described were found, together with five haplotypes known to be present in other parts of the world, including the haplotype EG01 which is widespread and present in all endemic regions. These data extend knowledge related to the geographical spread and host range of E. granulosus s.s. in a country such as Australia in which the parasite established around 200 years ago.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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.)

Footnotes

These authors have contributed equally to this work.

References

REFERENCES

Alvarez Rojas, C. A., Gauci, C. G. and Lightowlers, M. W. (2013). Antigenic differences between the EG95-related proteins from Echinococcus granulosus G1 and G6 genotypes: implications for vaccination. Parasite Immunology 35, 99102.Google Scholar
Alvarez Rojas, C. A., Romig, T. and Lightowlers, M. W. (2014). Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. International Journal for Parasitology 44, 918.Google Scholar
Boufana, B., Lahmar, S., Rebai, W., Ben Safta, Z., Jebabli, L., Ammar, A., Kachti, M., Aouadi, S. and Craig, P. S. (2014). Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 706714.Google Scholar
Boufana, B., Lett, W. S., Lahmar, S., Buishi, I., Bodell, A. J., Varcasia, A., Casulli, A., Beeching, N. J., Campbell, F., Terlizzo, M., McManus, D. P. and Craig, P. S. (2015). Echinococcus equinus and Echinococcus granulosus sensu stricto from the United Kingdom: genetic diversity and haplotypic variation. International Journal for Parasitology 45, 161166.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
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
Busi, M., Snabel, V., Varcasia, A., Garippa, G., Perrone, V., Liberato, C. d. and D'Amelio, S. (2007). Genetic variation within and between G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Veterinary Parasitology 150, 7583.Google Scholar
Carmena, D. and Cardona, G. A. (2013). Canine echinococcosis: global epidemiology and genotypic diversity. Acta Tropica 128, 441460.CrossRefGoogle ScholarPubMed
Casulli, A., Interisano, M., Sreter, T., Chitimia, L., Kirkova, Z., La Rosa, G. and Pozio, E. (2012). Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infection, Genetics and Evolution 12, 377383.Google Scholar
Chaligiannis, I., Maillard, S., Boubaker, G., Spiliotis, M., Saratsis, A., Gottstein, B. and Sotiraki, S. (2015). Echinococcus granulosus infection dynamics in livestock of Greece. Acta Tropica 150, 6470.Google Scholar
Clement, M., Posada, D. and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.Google Scholar
Corbett, L. K. (1995). The Dingo in Australia and Asia. Comstock/Cornell, the University of Michigan.Google Scholar
Gemmell, M. A. (1990). Australasian contributions to an understanding of the epidemiology and control of hydatid disease caused by Echinococcus granulosus – past, present and future. International Journal for Parasitology 20, 431456.Google Scholar
Grainger, H. J. and Jenkins, D. J. (1996). Transmission of hydatid disease to sheep from wild dogs in Victoria, Australia. International Journal for Parasitology 26, 12631270.Google Scholar
Hailemariam, Z., Nakao, M., Menkir, S., Lavikainen, A., Yanagida, T., Okamoto, M. and Ito, A. (2012). Molecular identification of unilocular hydatid cysts from domestic ungulates in Ethiopia: implications for human infections. Parasitology International 61, 375377.Google Scholar
Hobbs, R. P., Lymbery, A. J. and Thompson, R. C. A. (1990). Rostellar hook morphology of Echinococcus granulosus (Batsch, 1786) from natural and experimental Australian hosts, and its implications for strain recognition. Parasitology 101, 273281.Google Scholar
Hope, M., Bowles, J. and McManus, D. P. (1991). A reconsideration of the Echinococcus granulosus strain situation in Australia following RFLP analysis of cystic material. International Journal for Parasitology 21, 471475.CrossRefGoogle ScholarPubMed
Huttner, M., Nakao, M., Wassermann, T., Siefert, L., Boomker, J. D., Dinkel, A., Sako, Y., Mackenstedt, U., Romig, T. and Ito, A. (2008). Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 38, 861868.Google Scholar
Jenkins, D. J. (2005). Hydatid control in Australia: where it began, what we have achieved and where to from here. International Journal for Parasitology 35, 733740.Google Scholar
Jenkins, D. J. (2006). Echinococcus granulosus in Australia, widespread and doing well. Parasitology International 55, S203S206.Google Scholar
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. and Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.CrossRefGoogle ScholarPubMed
Konyaev, S. V., Yanagida, T., Ingovatova, G. M., Shoikhet, Y. N., Nakao, M., Sako, Y., Bondarev, A. Y. and Ito, A. (2012). Molecular identification of human echinococcosis in the Altai region of Russia. Parasitology International 61, 711714.Google Scholar
Konyaev, S. V., Yanagida, T., Nakao, M., Ingovatova, G. M., Shoykhet, Y. N., Bondarev, A. Y., Odnokurtsev, V. A., Loskutova, K. S., Lukmanova, G. I., Dokuchaev, N. E., Spiridonov, S., Alshinecky, M. V., Sivkova, T. N., Andreyanov, O. N., Abramov, S. A., Krivopalov, A. V., Karpenko, S. V., Lopatina, N. V., Dupal, T. A., Sako, Y. and Ito, A. (2013). Genetic diversity of Echinococcus spp. in Russia. Parasitology 140, 16371647.Google Scholar
Kumaratilake, L. M. and Thompson, R. C. A. (1983). A comparison of Echinococcus granulosus from different geographical areas of Australia using secondary cyst development in mice. International Journal for Parasitology 13, 509515.Google Scholar
Kumaratilake, L. M., Thompson, R. C. A. and Dunsmore, J. D. (1983). Comparative strobilar development of Echinococcus granulosus of sheep origin from different geographical areas of Australia in vivo and in vitro. International Journal for Parasitology 13, 151156.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.Google Scholar
Lymbery, A. J. and Thompson, R. C. A. (1988). Electrophoretic analysis of genetic variation in Echinococcus granulosus from domestic hosts in Australia. International Journal for Parasitology 18, 803811.CrossRefGoogle ScholarPubMed
Lymbery, A. J., Thompson, R. C. A. and Hobbs, R. P. (1990). Genetic diversity and genetic differentiation in Echinococcus granulosus (Batsch, 1786) from domestic and sylvatic hosts on the mainland of Australia. Parasitology 101, 283289.CrossRefGoogle ScholarPubMed
Ma, J., Wang, H., Lin, G., Craig, P. S., Ito, A., Cai, Z., Zhang, T., Han, X., Ma, X., Zhang, J., Liu, Y., Zhao, Y. and Wang, Y. (2012). Molecular identification of Echinococcus species from eastern and southern Qinghai, China, based on the mitochondrial cox1 gene. Parasitology Research 111, 179184.Google Scholar
Moro, P. L., Nakao, M., Ito, A., Schantz, P. M., Cavero, C. and Cabrera, L. (2009). Molecular identification of Echinococcus isolates from Peru. Parasitology International 58, 184186.Google Scholar
Nakao, M., Sako, Y., Yokoyama, N., Fukunaga, M. and Ito, A. (2000). Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415424.Google Scholar
Nakao, M., Li, T., Han, X., Ma, X., Xiao, N., Qiu, J., Wang, H., Yanagida, T., Mamuti, W., Wen, H., Moro, P. L., Giraudoux, P., Craig, P. S. and Ito, A. (2010). Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. International Journal for Parasitology 40, 379385.Google Scholar
Nakao, M., Yanagida, T., Konyaev, S., Lavikainen, A., Odnokurtsev, V. A., Zaikov, V. A. and Ito, A. (2013). Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 140, 16251636.Google Scholar
Parsonson, I. (1998). The Australian Ark: A History of Domesticated Animals in Australia. CSIRO, Australia.Google Scholar
Romig, T., Ebi, D. and Wassermann, M. (2015). Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology 213, 7684.Google Scholar
Sambrook, J. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.Google Scholar
Snabel, V., Altintas, N., D'Amelio, S., Nakao, M., Romig, T., Yolasigmaz, A., Gunes, K., Turk, M., Busi, M., Huttner, M., Sevcova, D., Ito, A., Altintas, N. and Dubinsky, P. (2009). Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitology Research 105, 145154.Google Scholar
Vural, G., Baca, A. U., Gauci, C. G., Bagci, O., Gicik, Y. and Lightowlers, M. W. (2008). Variability in the Echinococcus granulosus cytochrome C oxidase 1 mitochondrial gene sequence from livestock in Turkey and a re-appraisal of the G1–3 genotype cluster. Veterinary Parasitology 154, 347350.Google Scholar
Yanagida, T., Mohammadzadeh, T., Kamhawi, S., Nakao, M., Sadjjadi, S. M., Hijjawi, N., Abdel-Hafez, S. K., Sako, Y., Okamoto, M. and Ito, A. (2012). Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitology International 61, 599603.Google Scholar
Zhong, X., Wang, N., Hu, D., Wang, J., Liu, T., Gu, X., Wang, S., Peng, X. and Yang, G. (2014). Sequence analysis of cytb gene in Echinococcus granulosus from Western China. Korean Journal of Parasitology 52, 205209.Google Scholar