Hostname: page-component-5db58dd55d-8lnk4 Total loading time: 0 Render date: 2026-06-01T17:39:18.362Z Has data issue: false hasContentIssue false
  • English
  • Français

Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping

Published online by Cambridge University Press:  05 December 2013

E. KEATS SHWAB ,
XING-QUAN ZHU ,
DEBASHREE MAJUMDAR ,
HILDA F. J. PENA ,
SOLANGE M. GENNARI ,
JITENDER P. DUBEY  and
CHUNLEI SU
E. KEATS SHWAB
Affiliation:
Department of Microbiology, The University of Tennessee, Knoxville, TN 37996, USA
XING-QUAN ZHU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, People's Republic of China
DEBASHREE MAJUMDAR
Affiliation:
Department of Microbiology, The University of Tennessee, Knoxville, TN 37996, USA
HILDA F. J. PENA
Affiliation:
Faculty of Veterinary Medicine, University of São Paulo, São Paulo, Brazil
SOLANGE M. GENNARI
Affiliation:
Faculty of Veterinary Medicine, University of São Paulo, São Paulo, Brazil
JITENDER P. DUBEY
Affiliation:
Animal Parasitic Diseases Laboratory, United States Department of Agriculture, Beltsville, MD 20705, USA
CHUNLEI SU*
Affiliation:
Department of Microbiology, The University of Tennessee, Knoxville, TN 37996, USA State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, People's Republic of China
*
* Corresponding author: Department of Microbiology, The University of Tennessee, Knoxville, TN 37996, USA. E-mail: csu1@utk.edu
Get access Rights & Permissions [Opens in a new window]

Summary

In recent years, an extensive collection of Toxoplasma gondii samples have been typed using a set of 10 PCR-RFLP genetic markers. Here we summarize the data reported until the end of 2012. A total of 1457 samples were typed into 189 genotypes. Overall, only a few genotypes dominate in the northern hemisphere, which is in stark contrast to the southern hemisphere where hundreds of genotypes coexist with none being notably dominant. PCR-RFLP genotype #1 (Type II clonal), #2 (Type III), #3 (Type II variant) and #10 (Type I) are identified globally. Genotypes #2 and #3 dominate in Africa, genotypes #9 (Chinese 1) and #10 are prevalent in Asia, genotypes #1, #2 and #3 are prevalent in Europe, genotypes #1, #2, #3, #4 and #5 dominate in North America (#4 and #5 are collectively known as Type 12). In Central and South America, there is no clear dominance of any genotype even though a few have relatively higher frequencies. Statistical analysis indicates significant differences among populations in Africa, Asia, Europe, North America, and Central and South America, with only Europe and North America exhibiting similar diversity. Collectively, the results revealed distinct population structures and geographical patterns of diversity in T. gondii.

Keywords

Toxoplasma gondiiPCR-RFLPgenotypingpopulation structuregenetic diversity

Information

Type
Review Article
Information
Parasitology , Volume 141 , Issue 4 , April 2014 , pp. 453 - 461
Creative Commons
This is a work of the U.S. Government and is not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2013

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Ajzenberg, D., Bañuls, A. L., Tibayrenc, M. and Dardé, M. L. (2002). Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. International Journal for Parasitology 32, 27–38.CrossRefGoogle ScholarPubMed
Ajzenberg, D., Collinet, F., Mercier, A., Vignoles, P. and Dardé, M. L. (2010). Genotyping of Toxoplasma gondii isolates with 15 microsatellite markers in a single multiplex PCR assay. Journal of Clinical Microbiology 48, 4641–4645.CrossRefGoogle Scholar
Alvarado-Esquivel, C., Rajendran, C., Ferreira, L. R., Kwok, O. C., Choudhary, S., Alvarado-Esquivel, D., Rodríguez-Peña, S., Villena, I. and Dubey, J. P. (2011). Prevalence of Toxoplasma gondii infection in wild birds in Durango, Mexico. Journal of Parasitology 97, 809–812.CrossRefGoogle ScholarPubMed
Buxton, D., Maley, S. W., Wright, S. E., Rodger, S., Bartley, P. and Innes, E. A. (2007). Toxoplasma gondii and ovine toxoplasmosis: new aspects of an old story. Veterinary Parasitology 149, 25–28.Google Scholar
Chen, Z. W., Gao, J. M., Huo, X. X., Wang, L., Yu, L., Halm-Lai, F., Xu, Y. H., Song, W. J., Hide, G., Shen, J. L. and Lun, Z. R. (2011). Genotyping of Toxoplasma gondii isolates from cats in different geographic regions of China. Veterinary Parasitology 183, 166–170.CrossRefGoogle ScholarPubMed
Conrad, P. A., Miller, M. A., Kreuder, C., James, E. R., Mazet, J., Dabritz, H., Jessup, D. A., Gulland, F. and Grigg, M. E. (2005). Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. International Journal for Parasitology 35, 1155–1168.CrossRefGoogle Scholar
Dardé, M. L., Ajzenberg, D. and Su, C. (2014). Molecular epidemiology and population structure of Toxoplasma gondii . In Toxoplasma gondii – The Model Apicomplexan: Perspectives and Methods, 2nd Edn (ed. Weiss, L. M. and Kim, K.), pp. 61–97. Elsevier, San Diego, CA, USA.CrossRefGoogle Scholar
Diamond, J. and Bellwood, P. (2003). Farmers and their languages: the first expansions. Science 300, 597–603.CrossRefGoogle ScholarPubMed
Dubey, J. P. (2010). Toxoplasmosis of Animals and Humans, 2nd Edn. CRC Press, Boca Raton, FL, USA.Google Scholar
Dubey, J. P., Morales, J. A., Sundar, N., Velmurugan, G. V., González-Barrientos, C. R., Hernández-Mora, G. and Su, C. (2007 a). Isolation and genetic characterization of Toxoplasma gondii from striped dolphin (Stenella coeruleoalba) from Costa Rica. Journal of Parasitology 93, 710–711.CrossRefGoogle ScholarPubMed
Dubey, J. P., Zhu, X. Q., Sundar, N., Zhang, H., Kwok, O. C. H. and Su, C. (2007 b). Genetic and biologic characterization of Toxoplasma gondii isolates of cats from China. Veterinary Parasitology 145, 352–356.CrossRefGoogle ScholarPubMed
Dubey, J. P., Fair, P. A., Sundar, N., Velmurugan, G., Kwok, O. C. H., McFee, W. E., Majumdar, D. and Su, C. (2008). Isolation of Toxoplasma gondii from bottlenose dolphins (Tursiops truncatus). Journal of Parasitology 94, 821–823.CrossRefGoogle ScholarPubMed
Dubey, J. P., Passos, L. M. F., Rajendran, C., Ferreira, L. R., Gennari, S. M. and Su, C. (2011 a). Isolation of viable Toxoplasma gondii from feral guinea fowl (Numida meleagris) and domestic rabbits (Oryctolagus cuniculus) from Brazil. Journal of Parasitology 97, 842–845.CrossRefGoogle ScholarPubMed
Dubey, J. P., Velmurugan, G. V., Rajendran, C., Yabsley, M. J., Thomas, N. J., Beckmen, K. B., Sinnett, D., Ruid, D., Hart, J., Fair, P. A., McFee, E., Shearn-Bochsler, V., Kwok, O. C. H., Ferreira, L. R., Choudhary, S., Faria, E. B., Zhou, H., Felix, T. A. and Su, C. (2011 b). Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type. International Journal for Parasitology 41, 1139–1147.CrossRefGoogle ScholarPubMed
Excoffier, L. and Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Ferreira, A. d. M., Vitor, R. W., Gazzinelli, R. T. and Melo, M. N. (2006). Genetic analysis of natural recombinant Brazilian Toxoplasma gondii strains by multilocus PCR-RFLP. Infection, Genetics and Evolution 6, 22–31.CrossRefGoogle ScholarPubMed
Ferreira, I. M. R., Vidal, J. E., de Mattos, C. d. C. B., de Mattos, L. C., Qu, D., Su, C. and Pereira-Chioccola, V. L. (2011). Toxoplasma gondii isolates: multilocus RFLP-PCR genotyping from human patients in Sao Paulo State, Brazil identified distinct genotypes. Experimental Parasitology 129, 190–195.CrossRefGoogle Scholar
Gatkowska, J., Wieczorek, M., Dziadek, B., Dzitko, K. and Dlugonska, H. (2012). Sex-dependent neurotransmitter level changes in brains of Toxoplasma gondii infected mice. Experimental Parasitology 133, 1–7.Google Scholar
Grigg, M. E., Ganatra, J., Boothroyd, J. C. and Margolis, T. P. (2001). Unusual abundance of atypical strains associated with human ocular toxoplasmosis. Journal of Infectious Diseases 184, 633–639.CrossRefGoogle ScholarPubMed
Hamdani, N., Daban-Huard, C., Lajnef, M., Richard, J. R., Delavest, M., Godin, O., Le Guen, E., Vederine, F. E., Lépine, J. P., Jamain, S., Houenou, J., Le Corvoisier, P., Aoki, M., Moins-Teisserenc, H., Charron, D., Krishnamoorthy, R., Yolken, R., Dickerson, F., Tamouza, R. and Leboyer, M. (2013). Relationship between Toxoplasma gondii infection and bipolar disorder in a French sample. Journal of Affective Disorders 148, 444–448.CrossRefGoogle Scholar
Haroon, F., Handel, U., Angenstein, F., Goldschmidt, J., Kreutzmann, P., Lison, H., Fischer, K. D., Scheich, H., Wetzel, W., Schlüter, D. and Budinger, E. (2012). Toxoplasma gondii actively inhibits neuronal function in chronically infected mice. PLoS ONE 7, e35516.CrossRefGoogle ScholarPubMed
Howe, D. K. and Sibley, L. D. (1995). Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. Journal of Infectious Diseases 172, 1561–1566.CrossRefGoogle ScholarPubMed
Khan, A., Fux, B., Su, C., Dubey, J. P., Darde, M. L., Ajioka, J. W., Rosenthal, B. M. and Sibley, L. D. (2007). Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Proceedings of the National Academy of Sciences USA 104, 14872–14877.CrossRefGoogle ScholarPubMed
Khan, A., Dubey, J. B., Su, C., Ajioka, J. W., Rosenthal, B. M. and Sibley, L. D. (2011). Genetic analyses of atypical Toxoplasma gondii strains reveal a fourth clonal lineage in North America. International Journal for Parasitology 41, 645–655.CrossRefGoogle ScholarPubMed
Lehmann, T., Marcet, P. L., Graham, D. H., Dahl, E. R. and Dubey, J. P. (2006). Globalization and the population structure of Toxoplasma gondii . Proceedings of the National Academy of Sciences USA 103, 11423–11428.Google Scholar
Mercier, A., Devillard, S., Ngoubangoye, B., Bonnabau, H., Bañuls, A.-L., Durand, P., Salle, B., Ajzenberg, D. and Dardé, M.-L. (2010). Additional haplogroups of Toxoplasma gondii out of Africa: population structure and mouse-virulence of strains from Gabon. PLoS Neglected Tropical Diseases 4, e876.Google Scholar
Mercier, A., Ajzenberg, D., Devillard, S., Demar, M. P., de Thoisy, B., Bonnabau, H., Collinet, F., Boukhari, R., Blanchet, D., Simon, S., Carme, B. and Darde, M. L. (2011). Human impact on genetic diversity of Toxoplasma gondii: example of the anthropized environment from French Guiana. Infection, Genetics and Evolution 11, 1378–1387.CrossRefGoogle ScholarPubMed
Miller, M. A., Miller, W. A., Conrad, P. A., James, E. R., Melli, A. C., Leutenegger, C. M., Dabritz, H. A., Packham, A. E., Paradies, D., Harris, M., Ames, J., Jessup, D. A., Worcester, K. and Grigg, M. E. (2008). Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. International Journal for Parasitology 38, 1319–1328.CrossRefGoogle Scholar
Montoya, J. G. and Liesenfeld, O. (2004). Toxoplasmosis. Lancet 363, 1965–1976.Google Scholar
Pearce, B. D., Kruszon-Moran, D. and Jones, J. L. (2012). The relationship between Toxoplasma gondii infection and mood disorders in the third National Health and Nutrition Survey. Biological Psychiatry 72, 290–295.Google Scholar
Pena, H. F. J., Gennari, S. M., Dubey, J. P. and Su, C. (2008). Population structure and mouse-virulence of Toxoplasma gondii in Brazil. International Journal for Parasitology 38, 561–569.CrossRefGoogle ScholarPubMed
Rajendran, C., Su, C. and Dubey, J. P. (2012). Molecular genotyping of Toxoplasma gondii from Central and South America revealed high diversity within and between populations. Infection, Genetics and Evolution 12, 359–368.Google Scholar
Rengifo-Herrera, C., Ortega-Mora, L. M., Alvarez-García, G., Gómez-Bautista, M., García-Párraga, D., García-Peña, F. J. and Pedraza-Díaz, S. (2012). Detection of Toxoplasma gondii antibodies in Antarctic pinnipeds. Veterinary Parasitology 190, 259–262.Google Scholar
Rosenthal, B. M. (2009). How has agriculture influenced the geography and genetics of animal parasites? Trends in Parasitology 25, 67–70.Google Scholar
Su, C., Evans, D., Cole, R. H., Kissinger, J. C., Ajioka, J. W. and Sibley, L. D. (2003). Recent expansion of Toxoplasma through enhanced oral transmission. Science 299, 414–416.CrossRefGoogle ScholarPubMed
Su, C., Zhang, X. and Dubey, J. P. (2006). Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. International Journal for Parasitology 36, 841–848.CrossRefGoogle ScholarPubMed
Su, C., Shwab, E. K., Zhou, P., Zhu, X. Q. and Dubey, J. P. (2010). Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii . Parasitology 137, 1–11.CrossRefGoogle ScholarPubMed
Su, C., Khan, A., Zhou, P., Majumdar, D., Ajzenberg, D., Dardé, M. L., Zhu, X. Q., Ajioka, J. W., Rosenthal, B. M., Dubey, J. P. and Sibley, L. D. (2012). Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages. Proceedings of the National Academy of Sciences USA 109, 5844–5849.Google Scholar
Sundar, N., Cole, R. A., Thomas, N. J., Majumdar, D., Dubey, J. P. and Su, C. (2008). Genetic diversity among sea otter isolates of Toxoplasma gondii . Veterinary Parasitology 151, 125–132.Google Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.CrossRefGoogle ScholarPubMed
Torrey, E. F., Bartko, J. J. and Lun, Z. R. (2007). Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophrenia Bulletin 33, 729–736.CrossRefGoogle ScholarPubMed
Yolken, R. H., Bachmann, S., Ruslanova, I., Lillehoj, E., Ford, G., Torrey, E. F. and Schroeder, J. (2001). Antibodies to Toxoplasma gondii in individuals with first-episode schizophrenia. Clinical Infectious Diseases 32, 842–844.Google Scholar
Supplementary material: File

Shwab et al. Supplementary Material

Table S1

Download Shwab et al. Supplementary Material(File)
File 387.6 KB