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The use of DNA hybridization and numerical taxonomy in determining relationships between Trypanosoma brucei stocks and subspecies

  • P. Paindavoine (a1), E. Pays (a1), M. Laurent (a1), Y. Geltmeyer (a1), D. Le Ray (a2), D. Mehlitz (a3) and M. Steinert (a1)...

The nuclear DNAs of 71 trypanosome stocks from different African countries, representative of the three Trypanosoma brucei subspecies, and one T. evansi stock, have been analysed by the combined use of restriction endonuclease digestion, gel electrophoresis and molecular hybridization with both trypanosome surface-antigen-specific and undefined genomic DNA probes. In contrast with T. brucei brucei and T. brucei rhodesiense stocks, all the T. b. gambiense stocks are characterized by a conserved, specific DNA band pattern, regardless of the probe. This allows T. b. gambiense to be non-ambiguously identified. On the contrary, T. b. brucei and T. b. rhodesiense, which could not be discriminated by the same criteria, both yield highly variable DNA band patterns. Our data confirm that domestic animals like pig, dog and sheep constitute a potential reservoir for T. b. gambiense. Using a numerical analysis of the DNA hybridization patterns we have measured the degree of similarity between the 72 trypanosome stocks. This investigation shows that all T. b. gambiense stocks are included in the same homogeneous population, while the stocks from the two other subspecies seem to be distributed in several heterogeneous groups, some of these showing correlation with the geographical origin of the trypanosomes. It is concluded that (i) T. b. gambiense stands out as a real subspecies that has undergone a distinct evolution relative to the ‘non-gambiense’ group, (ii) the alleged T. b. rhodesiense subspecies does not fit with any of the groups evidenced by our cladistic analysis and hence does not appear as a distinct subspecies and (iii) ‘non-gambiense’ trypanosomes are probably evolving much more rapidly than T. b. gambiense. Different aspects of trypanosome relationships and evolution are discussed.

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Benton W. D. & Davis R. W. (1977). Screening gt recombinant clones by hybridization to single plaques in situ. Science 196, 180–2.
Bernards A., Michels P. A. M., Lincke C. R. & Borst P. (1983). Growth of chromosome ends in multiplying trypanosomes. Nature, London 303, 592–7.
Borst P. & Cross G. A. M. (1982). Molecular basis for trypanosome antigenic variation. Cell 29, 291303.
Borst P., Fase-Fowler F., Frasch A. C. C., Hoeijmakers J. H. J. & Weijers P. J. (1980 a). Characterization of DNA from Trypanosoma brucei and related trypanosomes by restriction endonuclease digestion. Molecular and Biochemical Parasitology 1, 221–46.
Borst P., Fase-Fowler F., Frasch A. C. C., Hoeijmakers J. H. J. & Weijers P. J. (1980 b). Variations in maxi-circle and mini-circle sequences in kinetoplast DNAs from different Trypanosoma brucei strains. Biochemica et Biophysica Acta 610, 197210.
Borst P., Fase-Fowler F., & Gibson W. C. (1981). Quantitation of genetic differences between Trypanosoma brucei gambiense, rhodesiense and brucei by restriction enzyme analysis of kinetoplast DNA. Molecular and Biochemical Parasitology 3, 117–31.
Denecke K. (1941). Menschenpathogene Trypanosomen des Hundes auf Feernando Poo. Ein Beitrag für Epidemiologie der Schlafkrankeit. Archiv für Hygiene und Bakteriologie 126, 3842.
Frasch A. C. C., Borst P. & Van den Burg J. (1982). Rapid evolution of genes coding for variant surface glycoproteins in trypanosomes. Gene 17, 197211.
Gibson W. C., Mehlitz D., Lanham S. M. & Godfrey D. G. (1978). The identification of T. brucei gambiense in Liberian pigs and dogs by isoenzymes and by resistance to human plasma. Tropenmedizin und Parasitologie 29, 335–45.
Gibson W. C., Marshall T. F. & Godfrey D. G. (1980). Numerical analysis of enzyme polymorphism: a new approach to the epidemiology and taxonomy of trypanosomes of the subgenus Trypanozoon. Advances in Parasitology 18, 175246.
Godfrey D. G. & Kilgour V. (1976). Enzyme electrophoresis in characterizing the causative organism of Gambian trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 219–24.
Hawking F. (1976). The resistance to human plasma of Trypanosoma brucei, T. rhodesience and T. gambiense. II. Survey of strains from East Africa and Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 513–20.
Hoare C. A. (1972). The Trypanosomes of Mammals. Oxford: Blackwell Scientific Publications.
Jaccard P. (1908). Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise des Sciences Naturelles 44, 223–70.
Kilgour V. & Godfrey D. G. (1973). Species-characteristic isoenzymes of two aminotransferases in trypanosomes. Nature, London 244, 6970.
Lanotte G., Rioux J. A., Maazoun R., Pasteur N., Pratlong F. & Lepart J. (1981). Application de la méthode numérique à la taxonomie du genre Leishmania, Ross 1903. Annales de Parasitologie 6, 575–92.
Latif B. M. A. & Adam K. M. G. (1973). Differentiation of T. brucei, T. rhodesiense and T. gambiense by the indirect fluorescent antibody test. Bulletin de l'Organisation Mondiale de la Santé 48, 401–7.
Laurent M., Pays E., Delinte K., Magnus E., Van Meirvenne N. & Steinert M. (1984 a). Evolution of a surface antigen gene repertoire is linked to a non-duplicative gene activation. Nature, London 308, 370–3.
Laurent M., Pays E., Magnus E., Van Meirvenne N., Matthyssens G., Williams R. D. & Steinert M. (1983). DNA rearrangements linked to expression of a predominant surface antigen gene of trypanosomes. Nature, London 302, 263–6.
Laurent M., Pays E., Van Der Werf A., Aerts D., Magnus E., Van Meirvenne N. & Steinert M. (1984 b). Translocation alters the activation rate of a trypanosome surface antigen gene. Nucleic Acids Research 12, 8319–28.
Le Ray D. (1975). Structures antigéniques de Trypanosoma brucei (Protozoa, Kinetoplastida). Analyse immunoélectrophorétique et étude comparative. Annales de la Société Belge de Médecine Tropicale 55, 129311.
Le Ray D., Afchain D., Jadin J., Capron A. & Fameree L. (1971). Interrelations immuno-taxonomiques de T. brucei, T. rhodesiense et T. gambiense. Annales de Parasitologie humaine et comparée 46, 523–32.
Massamba N. N. & Williams R. O. (1984). Distinction of African trypanosome species using nucleic acid hybridization. Parasitology 88, 5565.
Mehlitz D., Zillman U., Scott C. M. & Godfrey D. G. (1982). Epidemiological studies on the animal reservoir of gambiense sleeping sickness. Part III. Characterization of Trypanozoon stocks by isoenzymes and sensitivity to human serum. Tropenmedizin und Parasitologie 33, 113–18.
Pays E., Dekerck P., Van Assel S., Eldirdiri A. B., Le Ray D., Van Meirvenne N. & Steinert M. (1983 e). Comparative analysis of a Trypanosoma brucei gambiense antigen gene family and its potential use in epidemiology of sleeping sickness. Molecular and Biochemical Parasitology 7, 6374.
Pays E., Delauw M. F., Van Assel S., Laurent M., Vervoort T., Van Meirvenne N. & Steinert M. (1983 c). Modification of a Trypanosoma b. brucei antigen gene repertoire by different DNA recombinational mechanisms. Cell 35, 721–31.
Pays E., Delronche M., Lheureux M., Vervoort T., Bloch J., Gannon F. & Steinert M. (1980). Cloning and characterization of DNA sequences complementary to mRNAs coding for the synthesis of two surface antigens of Trypanosoma brucei. Nucleic Acids Research 8, 5965–81.
Pays E., Laurent M., Delinte K., Van Meirvenne N. & Steinert M. (1983 d). Differential size variations between transcriptionally active and inactive telomeres of Trypanosoma brucei. Nucleic Acids Research 11, 8137–47.
Pays E., Lheureux M. and Steinert M. (1982). Structure and expression of a Trypanosoma brucei gambiense variant-specific antigen gene. Nucleic Acids Research 10, 3149–63.
Pays E., Lheureux M., Vervoort T. & Steinert M. (1981). Conservation of a variant-specific surface antigen gene in different trypanosome species and subspecies. Molecular and Biochemical Parasitology 4, 349–57.
Pays E., Van Assel S., Laurent M., Darville M., Vervoort T., Van Meirvenne N. & Steinert M. (1983 b). Gene conversion as a mechanism for antigenic variation in trypanosomes. Cell, 34, 371–81.
Pays E., Van Assel S., Laurent M., Dero B., Michiels F., Kronenberger P., Matthyssens G., Van Meirvenne N., Le Ray D. & Steinert M. (1983 a). At least two transposed sequences are associated in the expression site of a surface antigen gene in different trypanosome clones. Cell 34, 359–69.
Pays E., Van Assel S., Le Ray D., Van Meirvenne N., Mehlitz D. & Steinert M. (1984). Discrimination of the T. b. gambiense subspecies by molecular hybridization with specific, cloned cDNA probes. In New Approaches to the Identification of Parasites and their Vectors (ed. Newton B. N. and Michal F.), pp. 217223. Basel: Tropical Diseases Research Series, Schwabe & Co. AG.
Rickman L. R. & Robson J. (1970). The testing of proven Trypanosoma brucei and T. rhodesiense strains by the blood incubation infectivity test. Bulletin of the World Health Organization 42, 911–16.
Rigby P. W. J., Dickmann M., Rhodes C. & Berg P. J. (1977). Labelling DNA to high specific activity in vitro by nick-translation with polymerase I. Journal of Molecular Biology 113, 237–51.
Scott C. M., Freizil J. L., Tundic A. & Godfrey D. G. (1983). The sheep as a potential reservoir of human trypanosomiasis in the Republic of Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 397401.
Sorensen T. (1948). A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons. Biologiske Skrifter 5, 1–34.
Southern E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98, 503–17.
Tait A. (1980). Evidence for diploidy and mating in trypanosomes. Nature, London 287, 536–8.
Tait A., Eldirdiri A. B. & Le Ray D. (1984). Enzyme variation in Trypanosoma brucei ssp. I. Evidence for the sub-speciation of T. brucei gambiense. Parasitology 89, 311–26.
Van Der Ploeg L. H. T., Liu A. Y. C. & Borst P. (1984). Structure of the growing telomeres of trypanosomes. Cell 36, 459–68.
Van Meirvenne N., Janssens P. G. & Magnus E. (1975). Antigenic variation in syringe-passaged populations of Trypanosoma brucei. I. Rationalization of the experimental approach. Annales de la Société belge de Médecine Tropicale 55, 123.
Van Meirvenne N., Magnus E. & Janssens P. G. (1976). The effect of normal human serum on trypanosomes of distinct antigenic type (ETat 1 to 12) isolated from a strain of Trypanosoma brucei rhodesiense. Annales de la Société belge de Médecine Tropicale 56, 5563.
Voller A., Bidwell D. & Bartlett A. (1975). A serological study on human Trypanosoma rhodesiense infections using a microscale enzyme linked immunosorbent assay. Tropenmedizin und Parasitologie 26, 247–51.
Zillmann U., Mehlitz D. & Sachs R. (1984). Identity of Trypanozoon stocks isolated from man and domestic dogs in Liberia. Tropenmedizin und Parasitologie 35, 105–8.
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