Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-20T04:26:02.069Z Has data issue: false hasContentIssue false
  • English
  • Français

Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1

Published online by Cambridge University Press:  06 May 2004

A. OBWALLER ,
R. SCHNEIDER ,
J. WALOCHNIK ,
B. GOLLACKNER ,
A. DEUTZ ,
K. JANITSCHKE ,
H. ASPÖCK  and
H. AUER
A. OBWALLER
Affiliation:
Department of Medical Parasitology, Clinical Institute of Hygiene and Medical Microbiology, University of Vienna, Kinderspitalgasse 15, A-1095 Vienna, Austria
R. SCHNEIDER
Affiliation:
Department of Medical Parasitology, Clinical Institute of Hygiene and Medical Microbiology, University of Vienna, Kinderspitalgasse 15, A-1095 Vienna, Austria
J. WALOCHNIK
Affiliation:
Department of Medical Parasitology, Clinical Institute of Hygiene and Medical Microbiology, University of Vienna, Kinderspitalgasse 15, A-1095 Vienna, Austria
B. GOLLACKNER
Affiliation:
Department of Surgery, University of Vienna, Vienna, Austria
A. DEUTZ
Affiliation:
Department of Veterinary Affairs, Graz, Austria
K. JANITSCHKE
Affiliation:
Robert Koch Institut, Berlin, Germany
H. ASPÖCK
Affiliation:
Department of Medical Parasitology, Clinical Institute of Hygiene and Medical Microbiology, University of Vienna, Kinderspitalgasse 15, A-1095 Vienna, Austria
H. AUER
Affiliation:
Department of Medical Parasitology, Clinical Institute of Hygiene and Medical Microbiology, University of Vienna, Kinderspitalgasse 15, A-1095 Vienna, Austria
Get access Rights & Permissions [Opens in a new window]

Abstract

Genetic analyses of Echinococcus granulosus isolates from different intermediate host species have demonstrated substantial levels of variation for some genotype (strain) clusters. To determine the range of genetic variability within and between genotypes we amplified and cloned partial cox1 and nadh1 genes from 16 isolates of E. granulosus from 4 continents. Furthermore, we sequenced different clones from a PCR product to analyse the intra-individual genetic variance. The findings showed a moderate degree of variance within single isolates and a significant degree of variance between the cluster of genotypes G1–G3 (sheep, Tasmanian sheep and buffalo strain), genotypes G4 (horse strain) and G5 (cattle strain) and the cluster of the genotypes G6 (camel strain) and G7 (pig strain). The variance of up to 2·2% within genotypes was relatively low compared with that of 4·3–15·7% among genotypes. The present results indicate that a re-examination of the classification of 5 genotypes of Echinococcus is warranted. Hence, our data highly support a re-evaluation of the taxonomy of the clades G1–G3, G4, G5, G6/7 and G8 (cervid strain) within the genus Echinococcus.

Keywords

Echinococcus granulosuscytochrome c oxidase-1 (cox-1)NADH dehydrogenase-1 (nadh1)molecular strain differentiationsequence heterogeneity
Type
Research Article
Information
Parasitology , Volume 128 , Issue 5 , May 2004 , pp. 569 - 575
Copyright
2004 Cambridge University Press

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

BARDONNET, K., PIARROUX, R., DIA, L., SCHNEEGANS, F., BEURDELEY, A., GODOT, V. & VUITTON, D. A. (2002). Combined eco-epidemiological and molecular biology approaches to assess Echinococcus granulosus transmission to humans in Mauritania: occurrence of the ‘camel’ strain and human cystic echinococcosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 383–386.CrossRefGoogle Scholar
BIRKY, C. W. (1996). Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144, 427–437.Google Scholar
BOWLES, J., BLAIR, D. & McMANUS, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle Scholar
BOWLES, J. & McMANUS, D. P. (1993). NADH dehydrogenase I gene sequences compared for species and strains of the genus Echinococcus. International Journal for Parasitology 23, 969–972.CrossRefGoogle Scholar
BOWLES, J., BLAIR, D. & McMANUS, D. P. (1994). Molecular genetic characterization of the cervid strain (‘northern form’) of Echinococcus granulosus. Parasitology 109, 215–221.CrossRefGoogle Scholar
ECKERT, J. & THOMPSON, R. C. (1997). Intraspecific variation of and related species with emphasis on their infectivity to humans. Acta Tropica 64, 19–34.CrossRefGoogle Scholar
ECKERT, J., CONRATHS, F. J. & TACKMANN, K. (2000). Echinococcosis: an emerging or re-emerging zoonosis? International Journal for Parasitology 30, 1283–1294.Google Scholar
FELSENSTEIN, J. (1993). PHYLIP (Phylogeny Interference Package) 3.55c. Distributed by the author.
FERGUSON-MILLER, S. & BABCOCK, G. T. (1996). Heme/copper terminal oxidases. Chemical Reviews 96, 2889–2907.CrossRefGoogle Scholar
GAREY, J. R. & WOLSTENHOLME, D. R. (1989). Platyhelminth mitochondrial DNA: evidence for early evolutionary origin of a tRNA(serAGN) that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. Journal of Molecular Evolution 28, 3743–3787.CrossRefGoogle Scholar
GASSER, R. B., ZHU, X. & McMANUS, D. P. (1998). Display of sequence variation in PCR-amplified mitochondrial DNA regions of Echinococcus by single-strand conformation polymorphism. Acta Tropica 71, 107–115.CrossRefGoogle Scholar
KAMENETZKY, L., GUTIERREZ, A. M., CANOVA, S. G., HAAG, K. L., GUARNERA, E. A., PARRA, A., GARCIA, G. E. & ROSENZVIT, M. C. (2002). Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infection Genetics and Evolution 2, 129–136.CrossRefGoogle Scholar
KEDRA, A. H., SWIDERSKI, Z., TKACH, V. V., DUBINSKY, P., PAWLOWSKI, Z., STEFANIAK, J. & PAWLOWSKI, J. (1999). Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia and Ukraine. A multicenter study. Acta Parasitologica 44, 248–254.Google Scholar
LAVIKAINEN, A., LEHTINEN, M. J., MERI, T., HIRVELA-KOSKI, V., MERI, S. (2003). Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127, 207–215.CrossRefGoogle Scholar
LE, T. H., PEARSON, M. S., BLAIR, D., DAI, N., ZHANG, L. H. & McMANUS, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97–112.CrossRefGoogle Scholar
MORGAN, J. A. & BLAIR, D. (1998). Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. International Journal for Parasitology 28, 493–502.CrossRefGoogle 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, 451–458.CrossRefGoogle Scholar
PARFAIT, B., RUSTIN, P., MUNNICH, A. & ROTIG, A. (1998). Co-amplification of nuclear pseudogenes and assessment of heteroplasmy of mitochondrial DNA mutations. Biochemical and Biophysical Research Communications 247, 57–59.CrossRefGoogle Scholar
RAWSON, P. D. & HILBISH, T. J. (1995). Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Molecular Biology and Evolution 12, 893–901.Google Scholar
SCHUURMAN, R., DEMETER, L., REICHELDERFER, P., TIJNAGEL, J., DE GROOT, T. & BOUCHER, C. (1999). Worldwide evaluation of DNA sequencing approaches for identification of drug resistance mutations in the human immunodeficiency virus type 1 reverse transcriptase. Journal of Clinical Microbiology 37, 2291–2296.Google Scholar
SPEKSNIJDER, A. G., KOWALCHUK, G. A., DE JONG, S., KLINE, E., STEPHEN, J. R. & LAANBROEK, H. J. (2001). Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Applied and Environmental Microbiology 67, 469–472.CrossRefGoogle Scholar
SUZUKI, M. T. & GIOVANNONI, S. J. (1996). Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Applied and Environmental Microbiology 62, 625–630.Google Scholar
THOMPSON, R. C., LYMBERY, A. J. & CONSTANTINE, C. C. (1995). Variation in Echinococcus: towards a taxonomic revision of the genus. Advances in Parasitology 35, 145–176.CrossRefGoogle Scholar
THOMPSON, R. C. A. & McMANUS, D. P. (2001). Aetiology: parasites and life cycles. In WHO/OIEManual on Echinococcosis in Humans and Animals: A Zoonosis of Global Concern (ed. Eckert, J., Gemmel, M. A., Mesin, F. X. & Pawlowski, Z.S. ), pp. 1–19. World Organisation for Animal Health (OIE), Paris.
THOMPSON, R. C. & McMANUS, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452–457.CrossRefGoogle Scholar
TURCEKOVA, L., SNABEL, V., D'AMELIO, S., BUSI, M. & DUBINSKY, P. (2003). Morphological and genetic characterization of Echinococcus granulosus in the Slovak Republic. Acta Tropica 85, 223–229.CrossRefGoogle Scholar
VAN HERWERDEN, L., BLAIR, D. & AGATSUMA, T. (2000). Multiple lineages of the mitochondrial gene NADH dehydrogenase subunit 1 (ND1) in parasitic helminths: implications for molecular evolutionary studies of facultatively anaerobic eukaryotes. Journal of Molecular Evolution 51, 339–352.CrossRefGoogle Scholar
WALLACE, D. C. (1999). Mitochondrial diseases in man and mouse. Science 283, 1482–1488.CrossRefGoogle Scholar
XIA, X. & XIE, Z. (2001). DAMBE: Software package for data analysis in molecular biology and evolution. Journal of Heredity 92, 371–373.CrossRefGoogle Scholar