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Genetic characterization of Toxoplasma gondii isolates from Portugal, Austria and Israel reveals higher genetic variability within the type II lineage

Published online by Cambridge University Press:  13 February 2015

S. K. VERMA
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, Maryland 20705-2350, USA
D. AJZENBERG
Affiliation:
Centre National de Référence (CNR) Toxoplasmose/Toxoplasma Biological Resource Center (BRC), Centre Hospitalier-Universitaire Dupuytren, Limoges 87042, France INSERM UMR 1094, Neuroépidémiologie Tropicale, Laboratoire de Parasitologie-Mycologie, Faculté de Médecine, Université de Limoges, Limoges 87025, France
A. RIVERA-SANCHEZ
Affiliation:
Department of Microbiology, University of Tennessee, Knoxville, Tennessee 37996-0845, USA
C. SU
Affiliation:
Department of Microbiology, University of Tennessee, Knoxville, Tennessee 37996-0845, USA
J. P. DUBEY*
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, Maryland 20705-2350, USA
*
*Corresponding author. USDA, ARS, APDL, BARC-East Bldg 1001, Beltsville, Maryland 20705, USA. E-mail: Jitender.Dubey@ars.usda.gov

Summary

This study compared genetic diversity of Toxoplasma gondii isolates from Portugal, Austria and Israel. For this, we genotyped 90 T. gondii isolates (16 from Portugal, 67 from Austria and 7 from Israel) using 10 nested PCR-restriction length polymorphism (RFLP) genetic markers and 15 microsatellite (MS) markers. By PCR-RFLP typing, 7 isolates from Portugal chickens were identified as type II (ToxoDB #1 or #3), 4 were type III (ToxoDB #2) and the remaining 4 isolates have unique genotype pattern were designated as ToxoDB #254. One mouse virulent isolate from a bovine fetus (Bos taurus) in Portugal was type I (ToxoDB #10) at all loci and designated as TgCowPr1. All 67 isolates from Austria and 7 from Israel were type II (ToxoDB #1 or #3). By MS typing, many additional genetic variations were revealed among the type II and type III isolates. Phylogenetic analysis showed that isolates from the same geographical locations tend to cluster together, and there is little overlapping of genotypes among different locations. This study demonstrated that the MS markers can provide higher discriminatory power to reveal association of genotypes with geographical locations. Future studies of the type II strains in Europe by these MS markers will be useful to reveal transmission patterns of the parasite.

Type
Research Article
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 2015

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References

REFERENCES

Ajzenberg, D., Bañuls, A. L., Tibayrenc, M. and Dardé, M. L. (2002 a). Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. International Journal for Parasitology 32, 2738.Google Scholar
Ajzenberg, D., Cogné, N., Paris, L., Bessières, M. H., Thulliez, P., Filisetti, D., Pelloux, H., Marty, P. and Dardé, M. L. (2002 b). Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. Journal of Infectious Diseases 186, 684689.Google Scholar
Ajzenberg, D., Bañuls, A. L., Su, C., Dumètre, A., Demar, M., Carme, B. and Dardé, M. L. (2004). Genetic diversity, clonality and sexuality in Toxoplasma gondii . International Journal for Parasitology 34, 11851196.Google Scholar
Ajzenberg, D., Yera, H., Marty, P., Paris, L., Dalle, F., Menotti, J., Aubert, D., Franck, J., Bessières, M. H., Quinio, D., Pelloux, H., Delhaes, L., Desbois, N., Thulliez, P., Robert-Gangneux, F., Kauffmann-Lacroix, C., Pujol, S., Rabodonirina, M., Bougnoux, M. E., Cuisenier, B., Duhamel, C., Duong, T. H., Filisetti, D., Flori, P., Gay-Andrieux, F., Pratlong, F., Nevez, G., Totet, A., Carme, B., Bonnabau, H. et al. (2009). Genotype of 88 Toxoplasma gondii isolates associated with toxoplasmosis in immunocompromised patients, and correlation with clinical findings. Journal of Infectious Diseases 199, 11551177.Google Scholar
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, 46414645.Google Scholar
Aubert, D., Ajzenberg, D., Richomme, C., Gilot-Fromont, E., Terrier, M. E., de Gevigney, C., Game, Y., Maillard, D., Gibert, P., Dardé, M. L. and Villena, I. (2010). Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France. Veterinary Parasitology 171, 346349.Google Scholar
Canada, N., Meireles, C. S., Rocha, A., da Costa, J. M. C., Erickson, M. W. and Dubey, J. P. (2002). Isolation of viable Toxoplasma gondii from naturally infected aborted bovine fetuses. Journal of Parasitology 88, 12471248.Google Scholar
Carme, B., Ajzenberg, D., Demar, M., Simon, S., Dardé, M. L., Maubert, B. and de Thoisy, B. (2009). Outbreaks of toxoplasmosis in a captive breeding colony of squirrel monkeys. Veterinary Parasitology 163, 132135.Google Scholar
Costache, C. A., Colosi, H. A., Blaga, L., Gyorke, A., Pastiu, A. I., Colosi, I. A. and Ajzenberg, D. (2013). First isolation and genetic characterization of a Toxoplasma gondii strain from a symptomatic human case of congenital toxoplasmosis in Romania. Parasite 20, 11.Google Scholar
Craeye, S., Speybroeck, N., Ajzenberg, D., Dardé, M. L., Collinet, F., Tavernier, P., Van, G. S., Dorny, P. and Dierick, K. (2011). Toxoplasma gondii and Neospora caninum in wildlife: common parasites in Belgian foxes and Cervidae? Veterinary Parasitology 178, 6469.Google Scholar
Darde, M. L., Bouteille, B. and Pestrealexandre, M. (1992). Isoenzyme Analysis of 35 Toxoplasma gondii isolates and the biological and epidemiologic implications. Journal of Parasitology 78, 786794.Google Scholar
Demar, M., Ajzenberg, D., Maubon, D., Djossou, F., Panchoe, D., Punwasi, W., Valery, N., Peneau, C., Daigre, J. L., Aznar, C., Cottrelle, B., Terzan, L., Dardé, M. L. and Carme, B. (2007). Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clinical Infectious Diseases 45, e88e95.Google Scholar
Dubey, J. P. (2010). Toxoplasmosis of animals and humans. CRC, Boca Raton, FL.Google Scholar
Dubey, J. P., Graham, D. H., Silva, D. S., Lehmann, T. and Bahia-Oliveira, L. M. G. (2003). Toxoplasma gondii isolates of free-ranging chickens from Rio de Janeiro, Brazil: mouse mortality, genotype, and oocyst shedding by cats. Journal of Parasitology 89, 851853.Google Scholar
Dubey, J. P., Salant, H., Sreekumar, C., Dahl, E., Vianna, M. C. B., Shen, S. K., Kwok, O. C. H., Spira, D., Hamburger, J. and Lehmann, T. (2004). High prevalence of Toxoplasma gondii in a commercial flock of chickens in Israel, and public health implications of free-range farming. Veterinary Parasitology 121, 317322.Google Scholar
Dubey, J. P., Edelhofer, R., Marcet, P., Vianna, M. C. B., Kwok, O. C. H. and Lehmann, T. (2005). Genetic and biologic characteristics of Toxoplasma gondii infections in free-range chickens from Austria. Veterinary Parasitology 133, 299306.Google Scholar
Dubey, J. P., Vianna, M. C. B., Sousa, S., Canada, N., Meireles, S., Correia da Costa, J. M., Marcet, P. L., Lehmann, T., Dardé, M. L. and Thulliez, P. (2006). Characterization of Toxoplasma gondii isolates in free-range chickens from Portugal. Journal of Parasitology 92, 184186.Google Scholar
Dubey, J. P., Lago, E. G., Gennari, S. M., Su, C. and Jones, J. L. (2012). Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 139, 13751424.Google Scholar
Edelhofer, R. (1994). Prevalence of antibodies against Toxoplasma gondii in pigs in Austria – an evaluation of data from 1982 and 1992. Parasitology Research 80, 642644.Google Scholar
Edelhofer, R. and Prossinger, H. (2010). Infection with Toxoplasma gondii during pregnancy: seroepidemiological studies in Austria. Zoonoses and Public Health 57, 1826.Google Scholar
Elbez-Rubinstein, A., Ajzenberg, D., Dardé, M. L., Cohen, R., Dumètre, A., Yera, H., Gondon, E., Janaud, J. C. and Thulliez, P. (2009). Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. Journal of Infectious Diseases 199, 280285.Google Scholar
Fekkar, A., Ajzenberg, D., Bodaghi, B., Touafek, F., Le Hoang, P., Delmas, J., Robert, P. Y., Dardé, M. L., Mazier, D. and Paris, L. (2011). Direct genotyping of Toxoplasma gondii in ocular fluid samples from 20 patients with ocular toxoplasmosis: predominance of type II in France. Journal of Clinical Microbiology 49, 15131517.Google Scholar
Grigg, M. E. (2007). Population genetics, sex, and the emergence of clonal lines of Toxoplasma gondii . In Toxoplasma molecular and cellular biology (Eds. Ajioka, J. W., Soldati, D.), pp. 227240. Horizon Bioscience, Norfolk, UK.Google Scholar
Grigg, M. E. and Sundar, N. (2009). Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. International Journal for Parasitology 39, 925933.Google Scholar
Halos, L., Thébault, A., Aubert, D., Thomas, M., Perret, C., Geers, R., Alliot, A., Escotte-Binet, S., Ajzenberg, D., Dardé, M. L., Durand, B., Boireau, P. and Villena, I. (2010). An innovative survey underlining the significant level of contamination by Toxoplasma gondii of ovine meat consumed in France. International Journal for Parasitology 40, 193200.CrossRefGoogle ScholarPubMed
Herrmann, D. C., Pantchev, N., Vrhovec, M. G., Barutzki, D., Wilking, H., Fröhlich, A., Lüder, C. G., Conraths, F. J. and Schares, G. (2010). Atypical Toxoplasma gondii genotypes identified in oocysts shed by cats in Germany. International Journal for Parasitology 40, 285292.Google Scholar
Herrmann, D. C., Bärwald, A., Maksimov, A., Pantchev, N., Vrhovec, M. G., Conraths, F. J. and Schares, G. (2012a). Toxoplasma gondii sexual cross in a single naturally infected feline host: generation of highly mouse-virulent and avirulent clones, genotypically different from clonal types I, II and III. Veterinary Research 43, 39.Google Scholar
Herrmann, D. C., Maksimov, P., Maksimov, A., Sutor, A., Schwarz, S., Jaschke, W., Schliephake, A., Denzin, N., Conraths, F. J. and Schares, G. (2012b). Toxoplasma gondii in foxes and rodents from the German Federal States of Brandenburg and Saxony-Anhalt: seroprevalence and genotypes. Veterinary Parasitology 185, 7885.Google Scholar
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, 15611566.Google Scholar
Howe, D. K., Honoré, S., Derouin, F. and Sibley, L. D. (1997). Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. Journal of Clinical Microbiology 35, 14111414.Google Scholar
Jokelainen, P. (2012). Endemic Toxoplasma gondii genotype II causes fatal infections in animal hosts in Europe – lessons learnt. In Toxoplasmosis – Recent Advances. (ed. Djakovic, O. D.), pp. 121126. INTECH-open, Rijeka, Croatia.Google Scholar
Khan, A., Su, C., German, M., Storch, G. A., Clifford, D. B. and Sibley, L. D. (2005). Genotyping of Toxoplasma gondii strains from immunocompromised patients reveals high prevalence of type I strains. Journal of Clinical Microbiology 43, 58815887.Google Scholar
Lopes, A. P., Dubey, J. P., Darde, M. L. and Cardoso, L. (2014). Epidemiological review of Toxoplasma gondii infection in humans and animals in Portugal. Parasitology 141, 16991708.Google Scholar
Maksimov, P., Zerweck, J., Dubey, J. P., Pantchev, N., Frey, C. F., Maksimov, A., Reimer, U., Schutkowski, M., Hosseininejad, M., Ziller, M., Conraths, F. J. and Schares, G. (2013). Serotyping of Toxoplasma gondii in cats (Felis domesticus) reveals predominance of type II infections in Germany. PLoS ONE 8, e80213.Google Scholar
McLeod, R., Boyer, K. M., Lee, D., Mui, E., Wroblewski, K., Karrison, T., Noble, A. G., Withers, S., Swisher, C. N., Heydemann, P. T., Sautter, M., Babiarz, J., Rabiah, P., Meier, P., Grigg, M. E. and the Toxoplasmosis Study Group (2012). Prematurity and severity are associated with Toxoplasma gondii alleles (NCCCTS, 1981–2009). Clinical Infectious Diseases 54, 15951605.Google Scholar
Mercier, A., Devillard, S., Ngoubangoye, B., Bonnabau, H., Banuls, A. L., Durand, P., Salle, B., Ajzenberg, D. and Darde, 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
Mondragon, R., Howe, D. K., Dubey, J. P. and Sibley, L. D. (1998). Genotypic analysis of Toxoplasma gondii isolates from pigs. Journal of Parasitology 84, 639641.Google Scholar
Prestrud, K. W., Åsbakk, K., Mørk, T., Fuglei, E., Tryland, M. and Su, C. (2008). Direct high-resolution genotyping of Toxoplasma gondii in arctic foxes (Vulpes lagopus) in the remote arctic Svalbard archipelago reveals widespread clonal Type II lineage. Veterinary Parasitology 158, 121128.Google Scholar
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, 356368.Google Scholar
Richomme, C., Aubert, D., Gilot-Fromont, E., Ajzenberg, D., Mercier, A., Ducrot, C., Ferté, H., Delorme, D. and Villena, I. (2009). Genetic characterization of Toxoplasma gondii from wild boar (Sus scrofa) in France. Veterinary Parasitology 164, 296300.Google Scholar
Robert-Gangneux, F. and Dardé, M. L. (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clinical Microbiology Reviews 25, 264296.Google Scholar
Rosenberg, M. S. and Anderson, C. D. (2010). PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. In. Methods in Ecology and Evolution 2, 229232.Google Scholar
Saeij, J. P. J., Boyle, J. P., Coller, S., Taylor, S., Sibley, L. D., Brooke-Powell, E. T., Ajioka, J. W. and Boothroyd, J. C. (2006). Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314, 17801783.Google Scholar
Shwab, E. K., Zhu, X. Q., Majumdar, D., Pena, H. F. J., Gennari, S. M., Dubey, J. P. and Su, C. (2014). Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141, 453461.CrossRefGoogle ScholarPubMed
Sibley, L. D. and Ajioka, J. W. (2008). Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annual Review of Microbiology 62, 329351.Google Scholar
Sousa, S., Ajzenberg, D., Canada, N., Freire, L., Correia da Costa, J. M., Dardé, M. L., Thulliez, P. and Dubey, J. P. (2006). Biologic and molecular characterization of Toxoplasma gondii isolates from pigs from Portugal. Veterinary Parasitology 135, 133136.Google Scholar
Sousa, S., Ajzenberg, D., Vilanova, M., Costa, J. and Dardé, M. L. (2008). Use of GRA6-derived synthetic polymorphic peptides in an immunoenzymatic assay to serotype Toxoplasma gondii in human serum samples collected from three continents. Clinical and Vaccine Immunology 15, 13801386.Google Scholar
Sousa, S., Canada, N., da Costa, J. M. C. and Dardé, M. L. (2010). Serotyping of naturally Toxoplasma gondii infected meat-producing animals. Veterinary Parasitology 169, 2428.Google Scholar
Stajner, T., Vasiljevic, Z., Vujic, D., Markovic, M., Ristic, G., Micic, D., Pasic, S., Ivovic, V., Ajzenberg, D. and Djurkovic-Djakovic, O. (2013). Atypical strain of Toxoplasma gondii causing fatal reactivation after hematopoietic stem cell transplantation in a patient with an underlying immunological deficiency. Journal of Clinical Microbiology 51, 26862690.Google Scholar
Su, C., Howe, D. K., Dubey, J. P., Ajioka, J. W. and Sibley, L. D. (2002). Identification of quantitative trait loci controlling acute virulence in Toxoplasma gondii . Proceedings of the National Academy of Sciences of the United States of America 99, 1075310758.Google Scholar
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, 111.Google Scholar
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 of the United States of America 109, 58445849.Google Scholar
Taylor, S., Barragan, A., Su, C., Fux, B., Fentress, S. J., Tang, K., Beatty, W. L., El Hajj, H., Jerome, M., Behnke, M. S., White, M., Wootton, J. C. and Sibley, L. D. (2006). A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii . Science 314, 17761780.Google Scholar
Vilares, A., Gargate, M. J., Ferreira, I., Martins, S., Julio, C., Waap, H., Angelo, H. and Gomes, J. P. (2014). Isolation and molecular characterization of Toxoplasma gondii isolated from pigeons and stray cats in Lisbon, Portugal. Veterinary Parasitology. 205, 506511.Google Scholar
Waap, H., Vilares, A., Rebelo, E., Gomes, S. and Ângelo, H. (2008). Epidemiological and genetic characterization of Toxoplasma gondii in urban pigeons from the area of Lisbon (Portugal). Veterinary Parasitology 157, 306309.Google Scholar