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Comparative evaluation of Giardia duodenalis sequence data

Published online by Cambridge University Press:  19 June 2007

C. M. WIELINGA  and
R. C. A. THOMPSON
C. M. WIELINGA
Affiliation:
WHO Collaborating Centre for the Molecular Epidemiology of Parasitic Infections and the State Agricultural Biotechnology Centre, School of Veterinary and Biomedical Sciences, Murdoch University, South Street, Murdoch, Western Australia 6150, Australia
R. C. A. THOMPSON*
Affiliation:
WHO Collaborating Centre for the Molecular Epidemiology of Parasitic Infections and the State Agricultural Biotechnology Centre, School of Veterinary and Biomedical Sciences, Murdoch University, South Street, Murdoch, Western Australia 6150, Australia
*
*Corresponding author. Tel: +61 08 9360 2466. Fax: +61 08 9310 4144. E-mail: [email protected]
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Summary

A review of the Giardia duodenalis sequences currently available on the GenBank database was completed to compare the different genotyping loci (small subunit ribosomal DNA, glutamate dehydrogenase, triose-phosphate isomerase and beta giardin) for their ability to discern assemblage and subassemblage groups and infer phylogenetic relationships. In total, 405 Giardia duodenalis sequences were sorted and aligned to examine the substitutions within and between the assemblages – A and B (zoonotic), C and D (dogs), E (livestock), F (cats) and G (rodents). It was found that all of the genes could reproducibly group isolates into their assemblages and that the AI/AII subassemblage groups were robust and identifiable at all loci. However, the assemblage B subgroups were not reproducible at half of the loci (small subunit ribosomal DNA and beta giardin), not due to their conserved nature, but because there was insufficient sequence data of reference isolates available for comparison. It is anticipated that further investigation of these loci may reveal the core subgroups of this medically important and zoonotic assemblage and also those of others. The closer, more recent, phylogenetic relationships amongst the assemblages appear to be resolved; however, more sequence data from the current loci, and possibly new loci, will be required to establish the remaining relationships.

Keywords

GiardiagenotypingSSU rDNAgdhtpiβ giardinef1αconsensus sequencesphylogenetics
Type
Research Article
Information
Parasitology , Volume 134 , Issue 12 , November 2007 , pp. 1795 - 1821
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Abe, N., Kimata, I. and Tokoro, M. (2005 a). Genotyping of Giardia isolates from humans in Japan using the small subunit ribosomal RNA and glutamate dehydrogenase gene sequences. Japanese Journal of Infectious Diseases 58, 57–58.Google Scholar
Abe, N., Read, C., Thompson, R. C. and Iseki, M. (2005 b). Zoonotic genotype of Giardia intestinalis detected in a ferret. The Journal of Parasitology 91, 179–182.Google Scholar
Adam, R. D. (1992). Chromosome-size variation in Giardia lamblia: the role of rDNA repeats. Nucleic Acids Research 20, 3057–3061.CrossRefGoogle ScholarPubMed
Adam, R. D. (2001). Biology of Giardia lamblia. Clinical Microbiology Reviews 14, 447–475.CrossRefGoogle ScholarPubMed
Adam, R. D., Aggarwal, A., Lal, A. A., De La Cruz, V. F., McCutchan, T. and Nash, T. E. (1988). Antigenic variation of a cysteine-rich protein in Giardia lamblia. Journal of Experimental Medicine 167, 109–118.CrossRefGoogle ScholarPubMed
Adam, R. D., Yang, Y. M. and Nash, T. E. (1992). The cysteine-rich protein gene family of Giardia lamblia: loss of the CRP170 gene in an antigenic variant. Molecular and Cellular Biology 12, 1194–1201.Google Scholar
Amar, C. F., Dear, P. H., Pedraza-Diaz, S., Looker, N., Linnane, E. and McLauchlin, J. (2002). Sensitive PCR-restriction fragment length polymorphism assay for detection and genotyping of Giardia duodenalis in human feces. Journal of Clinical Microbiology 40, 446–452.Google Scholar
Andrews, R. H., Adams, M., Boreham, P. F., Mayrhofer, G. and Meloni, B. P. (1989). Giardia intestinalis: electrophoretic evidence for a species complex. International Journal for Parasitology 19, 183–190.CrossRefGoogle ScholarPubMed
Baruch, A. C., Isaac-Renton, J. and Adam, R. D. (1996). The molecular epidemiology of Giardia lamblia: a sequence-based approach. The Journal of Infectious Diseases 174, 233–236.CrossRefGoogle ScholarPubMed
Berrilli, F., Di Cave, D., De Liberato, C., Franco, A., Scaramozzino, P. and Orecchia, P. (2004). Genotype characterisation of Giardia duodenalis isolates from domestic and farm animals by SSU-rRNA gene sequencing. Veterinary Parasitology 122, 193–199.CrossRefGoogle ScholarPubMed
Binz, N., Thompson, R. C., Lymbery, A. J. and Hobbs, R. P. (1992). Comparative studies on the growth dynamics of two genetically distinct isolates of Giardia duodenalis in vitro. International Journal for Parasitology 22, 195–202.CrossRefGoogle ScholarPubMed
Boothroyd, J. C., Wang, A., Campbell, D. A. and Wang, C. C. (1987). An unusually compact ribosomal DNA repeat in the protozoan Giardia lamblia. Nucleic Acids Research 15, 4065–4084.CrossRefGoogle ScholarPubMed
Buchanan, B., Gruissem, W. and Jones, R. (2000). Biochemistry and Molecular Biology of Plants, American Society of Plant Physiologists Maryland, USA.Google Scholar
Caccio, S. M., De Giacomo, M. and Pozio, E. (2002). Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. International Journal for Parasitology 32, 1023–1030.Google Scholar
Caccio, S. M., Thompson, R. C., McLauchlin, J. and Smith, H. V. (2005). Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology 21, 430–437.Google Scholar
Edlind, T. D. and Chakraborty, P. R. (1987). Unusual ribosomal RNA of the intestinal parasite Giardia lamblia. Nucleic Acids Research 15, 7889–7901.CrossRefGoogle ScholarPubMed
Erlandsen, S. L. and Bemrick, W. J. (1987). SEM evidence for a new species, Giardia psittaci. The Journal of Parasitology 73, 623–629.CrossRefGoogle ScholarPubMed
Erlandsen, S. L., Bemrick, W. J., Wells, C. L., Feely, D. E., Knudson, L., Campbell, S. R., Van Keulen, H. and Jarroll, E. L. (1990). Axenic culture and characterization of Giardia ardeae from the great blue heron (Ardea herodias). The Journal of Parasitology 76, 717–724.CrossRefGoogle ScholarPubMed
Ey, P. L., Andrews, R. H. and Mayrhofer, G. (1993). Differentiation of major genotypes of Giardia intestinalis by polymerase chain reaction analysis of a gene encoding a trophozoite surface antigen. Parasitology 106, 347–356.CrossRefGoogle ScholarPubMed
Ey, P. L., Khanna, K., Andrews, R. H., Manning, P. A. and Mayrhofer, G. (1992). Distinct genetic groups of Giardia intestinalis distinguished by restriction fragment length polymorphisms. Journal of General Microbiology 138, 2629–2637.CrossRefGoogle ScholarPubMed
Ey, P. L., Mansouri, M., Kulda, J., Nohynkova, E., Monis, P. T., Andrews, R. H. and Mayrhofer, G. (1997). Genetic analysis of Giardia from hoofed farm animals reveals artiodactyl-specific and potentially zoonotic genotypes. The Journal of Eukaryotic Microbiology 44, 626–635.CrossRefGoogle ScholarPubMed
Fayer, R., Santin, M., Trout, J. M. and Dubey, J. P. (2006). Detection of Cryptosporidium felis and Giardia duodenalis Assemblage F in a cat colony. Veterinary Parasitology 140, 44–53.CrossRefGoogle Scholar
Filice, F. P. (1952). Studies on the cytology and life history of a Giardia from the laboratory rat. University of California Publications in Zoology 57, 53–146.Google Scholar
Guy, R. A., Xiao, C. and Horgen, P. A. (2004). Real-time PCR assay for detection and genotype differentiation of Giardia lamblia in stool specimens. Journal of Clinical Microbiology 42, 3317–3320.CrossRefGoogle ScholarPubMed
Healey, A., Mitchell, R., Upcroft, J. A., Boreham, P. F. and Upcroft, P. (1990). Complete nucleotide sequence of the ribosomal RNA tandem repeat unit from Giardia intestinalis. Nucleic Acids Research 18, 4006.Google Scholar
Holberton, D. V. and Marshall, J. (1995). Analysis of consensus sequence patterns in Giardia cytoskeleton gene promoters. Nucleic Acids Research 23, 2945–2953.Google Scholar
Homan, W. L., Van Enckevort, F. H., Limper, L., Van Eys, G. J., Schoone, G. J., Kasprzak, W., Majewska, A. C. and Van Knapen, F. (1992). Comparison of Giardia isolates from different laboratories by isoenzyme analysis and recombinant DNA probes. Parasitology Research 78, 316–323.CrossRefGoogle ScholarPubMed
Hopkins, R. M., Meloni, B. P., Groth, D. M., Wetherall, J. D., Reynoldson, J. A. and Thompson, R. C. (1997). Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. The Journal of Parasitology 83, 44–51.Google Scholar
Hunt, C. L., Ionas, G. and Brown, T. J. (2000). Prevalence and strain differentiation of Giardia intestinalis in calves in the Manawatu and Waikato regions of North Island, New Zealand. Veterinary Parasitology 91, 7–13.Google Scholar
Hunter, P. R. and Thompson, R. C. (2005). The zoonotic transmission of Giardia and Cryptosporidium. International Journal for Parasitology 35, 1181–1190.CrossRefGoogle ScholarPubMed
Itagaki, T., Kinoshita, S., Aoki, M., Itoh, N., Saeki, H., Sato, N., Uetsuki, J., Izumiyama, S., Yagita, K. and Endo, T. (2005). Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamate dehydrogenase gene sequencing. Veterinary Parasitology 133, 283–287.CrossRefGoogle ScholarPubMed
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.Google Scholar
Lalle, M., Jimenez-Cardosa, E., Caccio, S. M. and Pozio, E. (2005 a). Genotyping of Giardia duodenalis from humans and dogs from Mexico using a beta-giardin nested polymerase chain reaction assay. The Journal of Parasitology 91, 203–205.CrossRefGoogle ScholarPubMed
Lalle, M., Pozio, E., Capelli, G., Bruschi, F., Crotti, D. and Caccio, S. M. (2005 b). Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. International Journal for Parasitology 35, 207–213.CrossRefGoogle ScholarPubMed
Le Blancq, S. M., Kase, R. S. and Van Der Ploeg, L. H. (1991 a). Analysis of a Giardia lamblia rRNA encoding telomere with [TAGGG]n as the telomere repeat. Nucleic Acids Research 19, 5790.Google Scholar
Le Blancq, S. M., Korman, S. H. and Van Der Ploeg, L. H. (1991 b). Frequent rearrangements of rRNA-encoding chromosomes in Giardia lamblia. Nucleic Acids Research 19, 4405–4412.Google Scholar
Le Blancq, S. M., Korman, S. H. and Van Der Ploeg, L. H. (1992). Spontaneous chromosome rearrangements in the protozoan Giardia lamblia: estimation of mutation rates. Nucleic Acids Research 20, 4539–4545.Google Scholar
Leonhard, S., Pfister, K., Beelitz, P., Wielinga, C., Traub, R. and Thompson, R. C. A. (2006). The molecular characterisation of Giardia from dogs in Munich. In 22nd Annual Convention of the German Society for Parasitology, University of Veterinary Medicine Vienna, pp. 163, Abstract in programme.Google Scholar
Lu, S. Q., Baruch, A. C. and Adam, R. D. (1998). Molecular comparison of Giardia lamblia isolates. International Journal for Parasitology 28, 1341–1345.Google Scholar
Mahbubani, M. H., Bej, A. K., Perlin, M. H., Schaefer, F. W. 3rd, Jakubowski, W. and Atlas, R. M. (1992). Differentiation of Giardia duodenalis from other Giardia spp. by using polymerase chain reaction and gene probes. Journal of Clinical Microbiology 30, 74–78.CrossRefGoogle ScholarPubMed
Matsubayashi, M., Kimata, I. and Abe, N. (2005). Identification of genotypes of Giardia intestinalis isolates from a human and calf in Japan. The Journal of Veterinary Medical Science 67, 337–340.Google Scholar
Mayrhofer, G., Andrews, R. H., Ey, P. L. and Chilton, N. B. (1995). Division of Giardia isolates from humans into two genetically distinct assemblages by electrophoretic analysis of enzymes encoded at 27 loci and comparison with Giardia muris. Parasitology 111, 11–17.CrossRefGoogle ScholarPubMed
McArthur, A. G., Morrison, H. G., Nixon, J. E., Passamaneck, N. Q., Kim, U., Hinkle, G., Crocker, M. K., Holder, M. E., Farr, R., Reich, C. I., Olsen, G. E., Aley, S. B., Adam, R. D., Gillin, F. D. and Sogin, M. L. (2000). The Giardia genome project database. FEMS Microbiology Letters 189, 271–273.CrossRefGoogle ScholarPubMed
Meloni, B. P., Lymbery, A. J. and Thompson, R. C. (1988). Isoenzyme electrophoresis of 30 isolates of Giardia from humans and felines. The American Journal of Tropical Medicine and Hygiene 38, 65–73.Google Scholar
Meloni, B. P., Lymbery, A. J. and Thompson, R. C. (1989). Characterization of Giardia isolates using a non-radiolabeled DNA probe, and correlation with the results of isoenzyme analysis. The American Journal of Tropical Medicine and Hygiene 40, 629–637.CrossRefGoogle ScholarPubMed
Meloni, B. P. and Thompson, R. C. (1987). Comparative studies on the axenic in vitro cultivation of Giardia of human and canine origin: evidence for intraspecific variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 637–640.Google Scholar
Monis, P. T. and Andrews, R. H. (1998). Molecular epidemiology: assumptions and limitations of commonly applied methods. International Journal for Parasitology 28, 981–987.Google Scholar
Monis, P. T., Andrews, R. H., Mayrhofer, G. and Ey, P. L. (1999). Molecular systematics of the parasitic protozoan Giardia intestinalis. Molecular Biology and Evolution 16, 1135–1144.Google Scholar
Monis, P. T., Andrews, R. H., Mayrhofer, G. and Ey, P. L. (2003). Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 3, 29–38.Google Scholar
Monis, P. T., Andrews, R. H., Mayrhofer, G., Mackrill, J., Kulda, J., Isaac-Renton, J. L. and Ey, P. L. (1998). Novel lineages of Giardia intestinalis identified by genetic analysis of organisms isolated from dogs in Australia. Parasitology 116, 7–19.CrossRefGoogle ScholarPubMed
Monis, P. T., Mayrhofer, G., Andrews, R. H., Homan, W. L., Limper, L. and Ey, P. L. (1996). Molecular genetic analysis of Giardia intestinalis isolates at the glutamate dehydrogenase locus. Parasitology 112, 1–12.CrossRefGoogle ScholarPubMed
Mowatt, M. R., Weinbach, E. C., Howard, T. C. and Nash, T. E. (1994). Complementation of an Escherichia coli glycolysis mutant by Giardia lamblia triosephosphate isomerase. Experimental Parasitology 78, 85–92.CrossRefGoogle ScholarPubMed
Nash, T. (1992). Surface antigen variability and variation in Giardia lamblia. Parasitology Today 8, 229–234.Google Scholar
Nash, T. E. and Keister, D. B. (1985). Differences in excretory-secretory products and surface antigens among 19 isolates of Giardia. The Journal of Infectious Diseases 152, 1166–1171.CrossRefGoogle Scholar
Page, R. D. (1996). TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences. CABIOS 12, 357–358.Google Scholar
Read, C., Walters, J., Robertson, I. D. and Thompson, R. C. (2002). Correlation between genotype of Giardia duodenalis and diarrhoea. International Journal for Parasitology 32, 229–231.Google Scholar
Read, C. M., Monis, P. T. and Thompson, R. C. (2004). Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 4, 125–130.Google Scholar
Robertson, L. J., Hermansen, L., Gjerde, B. K., Strand, E., Alvsvag, J. O. and Langeland, N. (2006). Application of genotyping during an extensive outbreak of waterborne giardiasis in Bergen, Norway, during autumn and winter 2004. Applied and Environmental Microbiology 72, 2212–2217.Google Scholar
Roitt, I., Brostoff, J. and Male, D. (1996). Immunology, 4th Edn., Times Mirror International Publishers Limited London, UK.Google Scholar
Santin, M., Ludwig, K., Fayer, R. and Trout, J. M. (2003). First report of Giardia in coyotes (Canis latrans). The Journal of Eukaryotic Microbiology 50 (Suppl.) S709.CrossRefGoogle ScholarPubMed
Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. and Peattie, D. A. (1989). Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243, 75–77.CrossRefGoogle ScholarPubMed
Stranden, A. M., Eckert, J. and Kohler, P. (1990). Electrophoretic characterization of Giardia isolated from humans, cattle, sheep, and a dog in Switzerland. The Journal of Parasitology 76, 660–668.CrossRefGoogle Scholar
Sulaiman, I. M., Fayer, R., Bern, C., Gilman, R. H., Trout, J. M., Schantz, P. M., Das, P., Lal, A. A. and Xiao, L. (2003). Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerging Infectious Diseases 9, 1444–1452.Google Scholar
Sulaiman, I. M., Jiang, J., Singh, A. and Xiao, L. (2004). Distribution of Giardia duodenalis genotypes and subgenotypes in raw urban wastewater in Milwaukee, Wisconsin. Applied and Environmental Microbiology 70, 3776–3780.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.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, 4673–4680.Google Scholar
Thompson, R. C., Hopkins, R. M. and Homan, W. L. (2000). Nomenclature and genetic groupings of Giardia infecting mammals. Parasitology Today 16, 210–213.CrossRefGoogle ScholarPubMed
Thompson, R. C., Lymbery, A. J. and Meloni, B. P. (1990). Genetic variation in Giardia Kunstler, 1882: taxonomic and epidemiological significance. Protozoological Abstracts 14, 1–28.Google Scholar
Thompson, R. C. and Monis, P. T. (2004). Variation in Giardia: implications for taxonomy and epidemiology. Advances in Parasitology 58, 69–137.Google Scholar
Traub, R. J., Monis, P. T., Robertson, I., Irwin, P., Mencke, N. and Thompson, R. C. (2004). Epidemiological and molecular evidence supports the zoonotic transmission of Giardia among humans and dogs living in the same community. Parasitology 128, 253–262.Google Scholar
Trout, J. M., Santin, M. and Fayer, R. (2003). Identification of assemblage A Giardia in white-tailed deer. The Journal of Parasitology 89, 1254–1255.Google Scholar
Trout, J. M., Santin, M., Greiner, E. and Fayer, R. (2004). Prevalence of Giardia duodenalis genotypes in pre-weaned dairy calves. Veterinary Parasitology 124, 179–186.Google Scholar
Upcroft, J. A., Healey, A. and Upcroft, P. (1994). A new rDNA repeat unit in human Giardia. The Journal of Eukaryotic Microbiology 41, 639–642.Google Scholar
Upcroft, J. A. and Upcroft, P. (1994). Two distinct varieties of Giardia in a mixed infection from a single human patient. The Journal of Eukaryotic Microbiology 41, 189–194.CrossRefGoogle Scholar
Van Der Giessen, J. W., De Vries, A., Roos, M., Wielinga, P., Kortbeek, L. M. and Mank, T. G. (2006). Genotyping of Giardia in Dutch patients and animals: a phylogenetic analysis of human and animal isolates. International Journal for Parasitology 36, 849–858.Google Scholar
Van Keulen, H., Campbell, S. R., Erlandsen, S. L. and Jarroll, E. L. (1991). Cloning and restriction enzyme mapping of ribosomal DNA of Giardia duodenalis, Giardia ardeae and Giardia muris. Molecular and Biochemical Parasitology 46, 275–284.Google Scholar
Van Keulen, H., Feely, D. E., Macechko, P. T., Jarroll, E. L. and Erlandsen, S. L. (1998). The sequence of Giardia small subunit rRNA shows that voles and muskrats are parasitized by a unique species Giardia microti. The Journal of Parasitology 84, 294–300.Google Scholar
Van Keulen, H., Gutell, R. R., Gates, M. A., Campbell, S. R., Erlandsen, S. L., Jarroll, E. L., Kulda, J. and Meyer, E. A. (1993). Unique phylogenetic position of Diplomonadida based on the complete small subunit ribosomal RNA sequence of Giardia ardeae, G. muris, G. duodenalis and Hexamita sp. The FASEB Journal 7, 223–231.Google Scholar
Van Keulen, H., Homan, W. L., Erlandsen, S. L. and Jarroll, E. L. (1995). A three nucleotide signature sequence in small subunit rRNA divides human Giardia in two different genotypes. The Journal of Eukaryotic Microbiology 42, 392–394.Google Scholar
Van Keulen, H., Macechko, P. T., Wade, S., Schaaf, S., Wallis, P. M. and Erlandsen, S. L. (2002). Presence of human Giardia in domestic, farm and wild animals, and environmental samples suggests a zoonotic potential for giardiasis. Veterinary Parasitology 108, 97–107.CrossRefGoogle ScholarPubMed
Weiss, J. B., Van Keulen, H. and Nash, T. E. (1992). Classification of subgroups of Giardia lamblia based upon ribosomal RNA gene sequence using the polymerase chain reaction. Molecular and Biochemical Parasitology 54, 73–86.Google Scholar
Yee, J. and Dennis, P. P. (1992). Isolation and characterization of a NADP-dependent glutamate dehydrogenase gene from the primitive eucaryote Giardia lamblia. The Journal of Biological Chemistry 267, 7539–7544.Google Scholar
Yong, T. S., Park, S. J., Hwang, U. W., Yang, H. W., Lee, K. W., Min, D. Y., Rim, H. J., Wang, Y. and Zheng, F. (2000). Genotyping of Giardia lamblia isolates from humans in China and Korea using ribosomal DNA Sequences. The Journal of Parasitology 86, 887–891.Google Scholar