Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-25T13:17:50.328Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  06 April 2009

P. Paindavoine ,
E. Pays ,
M. Laurent ,
Y. Geltmeyer ,
D. Le Ray ,
D. Mehlitz  and
M. Steinert
P. Paindavoine
Affiliation:
Université Libre de Bruxelles, Département de Biologie Moléculaire, Rhode-St-Genèse, Belgium
E. Pays
Affiliation:
Université Libre de Bruxelles, Département de Biologie Moléculaire, Rhode-St-Genèse, Belgium
M. Laurent
Affiliation:
Université Libre de Bruxelles, Département de Biologie Moléculaire, Rhode-St-Genèse, Belgium
Y. Geltmeyer
Affiliation:
Université Libre de Bruxelles, Département de Biologie Moléculaire, Rhode-St-Genèse, Belgium
D. Le Ray
Affiliation:
Institute for Tropical Medicine, Department of Protozoology, Antwerp, Belgium
D. Mehlitz
Affiliation:
Bernhard-Nocht-Institut für Schiffs-und Tropenkrankheiten, Abteilung für Veterinärmedizin, Hamburg, West Germany
M. Steinert
Affiliation:
Université Libre de Bruxelles, Département de Biologie Moléculaire, Rhode-St-Genèse, Belgium
Get access Rights & Permissions [Opens in a new window]

Summary

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.

Type
Research Article
Information
Parasitology , Volume 92 , Issue 1 , February 1986 , pp. 31 - 50
Copyright
Copyright © Cambridge University Press 1986

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

Benton, W. D. & Davis, R. W. (1977). Screening gt recombinant clones by hybridization to single plaques in situ. Science 196, 180–2.Google Scholar
Bernards, A., Michels, P. A. M., Lincke, C. R. & Borst, P. (1983). Growth of chromosome ends in multiplying trypanosomes. Nature, London 303, 592–7.Google Scholar
Borst, P. & Cross, G. A. M. (1982). Molecular basis for trypanosome antigenic variation. Cell 29, 291–303.Google Scholar
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.Google Scholar
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, 197–210.Google Scholar
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.CrossRefGoogle ScholarPubMed
Denecke, K. (1941). Menschenpathogene Trypanosomen des Hundes auf Feernando Poo. Ein Beitrag für Epidemiologie der Schlafkrankeit. Archiv für Hygiene und Bakteriologie 126, 38–42.Google Scholar
Frasch, A. C. C., Borst, P. & Van den Burg, J. (1982). Rapid evolution of genes coding for variant surface glycoproteins in trypanosomes. Gene 17, 197–211.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 175–246.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals. Oxford: Blackwell Scientific Publications.Google Scholar
Jaccard, P. (1908). Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise des Sciences Naturelles 44, 223–70.Google Scholar
Kilgour, V. & Godfrey, D. G. (1973). Species-characteristic isoenzymes of two aminotransferases in trypanosomes. Nature, London 244, 69–70.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 129–311.Google Scholar
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.CrossRefGoogle Scholar
Massamba, N. N. & Williams, R. O. (1984). Distinction of African trypanosome species using nucleic acid hybridization. Parasitology 88, 55–65.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 63–74.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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. 217–223. Basel: Tropical Diseases Research Series, Schwabe & Co. AG.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 397–401.Google Scholar
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.Google Scholar
Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98, 503–17.CrossRefGoogle ScholarPubMed
Tait, A. (1980). Evidence for diploidy and mating in trypanosomes. Nature, London 287, 536–8.Google Scholar
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.CrossRefGoogle Scholar
Van Der Ploeg, L. H. T., Liu, A. Y. C. & Borst, P. (1984). Structure of the growing telomeres of trypanosomes. Cell 36, 459–68.Google Scholar
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, 1–23.Google Scholar
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, 55–63.Google Scholar
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.Google Scholar
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.Google Scholar