Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-23T10:27:26.678Z Has data issue: false hasContentIssue false
  • English
  • Français

New Trypanosoma (Duttonella) vivax genotypes from tsetse flies in East Africa

Published online by Cambridge University Press:  07 December 2009

E. R. ADAMS ,
P. B. HAMILTON ,
A. C. RODRIGUES ,
I. I. MALELE ,
V. DELESPAUX ,
M. M. G. TEIXEIRA  and
W. GIBSON
E. R. ADAMS
Affiliation:
School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK Koninklijk Instituut voor de Tropen (KIT) Biomedical Research, Amsterdam, Netherlands
P. B. HAMILTON
Affiliation:
School of Biosciences, University of Exeter, ExeterEX4 4PS, UK
A. C. RODRIGUES
Affiliation:
Departamento de Parasitologia, Universidade de Sao Paulo, Sao Paulo, Brazil
I. I. MALELE
Affiliation:
Tsetse and Trypanosomiasis Research Institute, PO Box 1026, Tanga, Tanzania
V. DELESPAUX
Affiliation:
Department of Animal Health, Institute of Tropical Medicine, B-2000Antwerp, Belgium
M. M. G. TEIXEIRA
Affiliation:
Departamento de Parasitologia, Universidade de Sao Paulo, Sao Paulo, Brazil
W. GIBSON*
Affiliation:
School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK
*
*Corresponding author: School of Biological Sciences, University of Bristol, BristolBS8 1UG, UK. Tel: +0117 928 8249. Fax: +0117 331 7985. E-mail: w.gibson@bris.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Salivarian trypanosomes pose a substantial threat to livestock, but their full diversity is not known. To survey trypanosomes carried by tsetse in Tanzania, DNA samples from infected proboscides of Glossina pallidipes and G. swynnertoni were identified using fluorescent fragment length barcoding (FFLB), which discriminates species by size polymorphisms in multiple regions of the ribosomal RNA locus. FFLB identified the trypanosomes in 65 of 105 (61·9%) infected proboscides, revealing 9 mixed infections. Of 7 different FFLB profiles, 2 were similar but not identical to reference West African Trypanosoma vivax; 5 other profiles belonged to known species also identified in fly midguts. Phylogenetic analysis of the glycosomal glyceraldehyde phosphate dehydrogenase gene revealed that the Tanzanian T. vivax samples fell into 2 distinct groups, both outside the main clade of African and South American T. vivax. These new T. vivax genotypes were common and widespread in tsetse in Tanzania. The T. brucei-like trypanosome previously described from tsetse midguts was also found in 2 proboscides, demonstrating a salivarian transmission route. Investigation of mammalian host range and pathogenicity will reveal the importance of these new trypanosomes for the epidemiology and control of animal trypanosomiasis in East Africa.

Keywords

fluorescent fragment length barcodingNaganaepidemiologylivestock diseasestrain typinggenotypingGlossinawhole genome amplificationspecies identificationphylogeny
Type
Research Article
Information
Parasitology , Volume 137 , Issue 4 , April 2010 , pp. 641 - 650
Copyright
Copyright © Cambridge University Press 2009

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

REFERENCES

Adams, E. R. (2008). The diversity, stability and prevalence of trypanosome infections from wild-caught tsetse flies in Tanzania. Ph.D. thesis, University of Bristol, Bristol, UK.Google Scholar
Adams, E. R., Hamilton, P. B., Malele, I. I. and Gibson, W. (2008). The identification, diversity and prevalence of trypanosomes in field caught tsetse in Tanzania using ITS-1 primers and fluorescent fragment length barcoding. Infection, Genetics and Evolution 8, 439–444.CrossRefGoogle ScholarPubMed
Adams, E. R., Malele, I. I., Msangi, A. R. and Gibson, W. C. (2006). Trypanosome identification in wild tsetse populations in Tanzania using generic primers to amplify the ribosomal RNA ITS-1 region Acta Tropica 100, 103–109.CrossRefGoogle ScholarPubMed
Bruford, M. W., Hanotte, O., Brookfield, J. F. and Burke, T. (1998). Multilocus and single-locus DNA fingerprinting. In Molecular Genetic Analysis of Populations: A Practical Approach (ed. Hoelzel, A. R.), pp. 287–336. IRL Press, Oxford, UK.CrossRefGoogle Scholar
Cortez, A. P., Rodrigues, A. C., Garcia, H. A., Neves, L., Batista, J. S., Bengaly, Z., Paiva, F. and Teixeira, M. M. G. (2009). Cathepsin L-like genes of Trypanosoma vivax from Africa and South America – characterization, relationships and diagnostic implications. Molecular and Cellular Probes 23, 44–51.CrossRefGoogle ScholarPubMed
Cortez, A. P., Ventura, R. M., Rodrigues, A. C., Batista, J. S., Paiva, F., Anez, N., Machado, R. Z., Gibson, W. C. and Teixeira, M. M. G. (2006). The taxonomic and phylogenetic relationships of Trypanosoma vivax from South America and Africa. Parasitology 133, 159–169.CrossRefGoogle ScholarPubMed
Dickin, S. K. and Gibson, W. C. (1989). Hybridization with a repetitive DNA probe reveals the presence of small chromosomes in Trypanosoma vivax. Molecular and Biochemical Parasitology 33, 135–142.CrossRefGoogle ScholarPubMed
Dirie, M. F., Murphy, N. B. and Gardiner, P. R. (1993 a). DNA fingerprinting of Trypanosoma vivax isolates rapidly identifies intraspecific relationships. Journal of Eukaryotic Microbiology 40, 132–134.CrossRefGoogle ScholarPubMed
Dirie, M. F., Otte, M. J., Thatthi, R. and Gardiner, P. R. (1993 b). Comparative studies of Trypanosoma (Duttonella) vivax isolates from Colombia. Parasitology 106, 21–29.CrossRefGoogle ScholarPubMed
Duffy, C. W., Morrison, L. J., Black, A., Pinchbeck, G. L., Christley, R. M., Schoenefeld, A., Tait, A., Turner, C. M. R. and MacLeod, A. (2009). Trypanosoma vivax displays a clonal population structure. International Journal for Parasitology (Published online June 2009).CrossRefGoogle ScholarPubMed
Fasogbon, A. I., Knowles, G. and Gardiner, P. R. (1990). A comparison of the isoenzymes of Trypanosoma (Duttonella) vivax isolates from East and West Africa. International Journal for Parasitology 20, 389–394.CrossRefGoogle ScholarPubMed
Gardiner, P. R. (1989). Recent studies of the biology of Trypanosoma vivax. Advances in Parasitology 28, 229–317.CrossRefGoogle ScholarPubMed
Gibson, W. (2007). Resolution of the species problem in African trypanosomes. International Journal for Parasitology 37, 829–838.CrossRefGoogle ScholarPubMed
Gibson, W. (2009). Species-specific probes for the identification of the African tsetse-transmitted trypanosomes. Parasitology (Published Online by Cambridge University Press 02 June 2009).CrossRefGoogle ScholarPubMed
Haag, J., O'Huigin, C. and Overath, P. (1998). The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 37–49.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Adams, E. R., Malele, I. I. and Gibson, W. C. (2008). A novel high throughput technique for species identification reveals a new species of tsetse-transmitted trypanosome related to the Trypanosoma brucei subgenus, Trypanozoon. Infection, Genetics and Evolution 8, 26–33.CrossRefGoogle Scholar
Hamilton, P. B., Adams, E. R., Njiokou, F., Gibson, W. C., Cuny, G. and Herder, S. (2009). Phylogenetic analysis reveals the presence of the Trypanosoma cruzi clade in African terrestrial mammals. Infection Genetics and Evolution 9, 81–86.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Gibson, W. C. and Stevens, J. R. (2007). Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Molecular Phylogenetics and Evolution 44, 15–25.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Stevens, J. R., Gaunt, M. W., Gidley, J. and Gibson, W. C. (2004). Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 1393–1404.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Stevens, J. R., Gidley, J., Holz, P. and Gibson, W. C. (2005). A new lineage of trypanosomes from Australian vertebrates and terrestrial bloodsucking leeches (Haemadipsidae). International Journal for Parasitology 35, 431–443.CrossRefGoogle ScholarPubMed
Hannaert, V., Opperdoes, F. R. and Michels, P. A. M. (1998). Comparison and evolutionary analysis of the glycosomal glyceraldehyde-3-phosphate dehydrogenase from different kinetoplastida. Journal of Molecular Evolution 47, 728–738.CrossRefGoogle ScholarPubMed
Hoare, C. A. (1972). The Trypanosomes of Mammals. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Jefferies, D., Helfrich, M. P. and Molyneux, D. H. (1987). Cibarial infections of Trypanosoma vivax and T. congolense in Glossina. Parasitology Research 73, 289–292.CrossRefGoogle Scholar
Lehane, M. J., Msangi, A. R., Whitaker, C. J. and Lehane, S. M. (2000). Grouping of trypanosome species in mixed infections in Glossina pallidipes. Parasitology 120, 583–592.CrossRefGoogle ScholarPubMed
Lloyd, L. and Johnson, W. B. (1924). The trypanosome infections of tsetse flies in northern Nigeria and a new method of estimation. Bulletin of Entomological Research 14, 265–288.CrossRefGoogle Scholar
Malele, I., Craske, L., Knight, C., Ferris, V., Njiru, Z., Hamilton, P., Lehane, S., Lehane, M. and Gibson, W. (2003). Identification of new trypanosome species from wild tsetse flies in Tanzania. Infection, Genetics and Evolution 3, 271–279.CrossRefGoogle ScholarPubMed
Masake, R. A., Majiwa, P. A. O., Moloo, S. K., Makau, J. M., Njuguna, J. T., Maina, M., Kabata, J., OleMoiYoi, O. K. and Nantulya, V. M. (1997). Sensitive and specific detection of Trypanosoma vivax using the polymerase chain reaction. Experimental Parasitology 85, 193–205.CrossRefGoogle ScholarPubMed
Masiga, D. K., Smyth, A. J., Hayes, P. J., Bromidge, T. J. and Gibson, W. C. (1992). Sensitive detection of trypanosomes in tsetse flies by DNA amplification. International Journal for Parasitology 22, 909–918.CrossRefGoogle ScholarPubMed
Morlais, I., Ravel, S., Grebaut, P., Dumas, V. and Cuny, G. (2001). New molecular marker for Trypanosoma (Duttonella) vivax identification. Acta Tropica 80, 207–213.CrossRefGoogle ScholarPubMed
Njiru, Z. K., Makumi, J. N., Okoth, S., Ndungu, J. M. and Gibson, W. C. (2004). Identification of trypanosomes in Glossina pallidipes and G. longipennis in Kenya. Infection, Genetics and Evolution 4, 29–35.CrossRefGoogle Scholar
Osorio, A. L. A. R., Madruga, C. R., Desquesnes, M., Soares, C. O., Ribeiro, L. R. R. and da Costa, S. C. G. (2008). Trypanosoma (Duttonella) vivax: its biology, epidemiology, pathogenesis, and introduction in the New World – a Review. Memorias do Instituto Oswaldo Cruz 103, 1–13.CrossRefGoogle ScholarPubMed
Rodrigues, A. C., Neves, L., Garcia, H. A., Viola, L. B., Marcili, A., Da Silva, F. M., Sigauque, I., Batista, J. S., Paiva, F. and Teixeira, M. M. G. (2008). Phylogenetic analysis of Trypanosoma vivax supports the separation of South American/West African from East African isolates and a new T. vivax-like genotype infecting a nyala antelope from Mozambique. Parasitology 135, 1317–1328.CrossRefGoogle Scholar
Stephen, L. E. (1986). Trypanosomiasis, a Veterinary Perspective. Pergamon Press, Oxford, UK.Google Scholar
Stevens, J. R., Noyes, H., Dover, G. A. and Gibson, W. C. (1999). The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2003). PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts, USA.Google Scholar