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Phylogeny, taxonomy and grouping of Trypanosoma rangeli isolates from man, triatomines and sylvatic mammals from widespread geographical origin based on SSU and ITS ribosomal sequences

Published online by Cambridge University Press:  05 October 2004

F. MAIA DA SILVA ,
H. NOYES ,
M. CAMPANER ,
A. C. V. JUNQUEIRA ,
J. R. COURA ,
N. AÑEZ ,
J. J. SHAW ,
J. R. STEVENS  and
M. M. G. TEIXEIRA
F. MAIA DA SILVA
Affiliation:
Department of Parasitology, Institute of Biomedical Science, University of São Paulo, São Paulo, SP, 05508-900, Brazil
H. NOYES
Affiliation:
Animal Genetics Laboratory, School of Biological Sciences, Donnan Laboratories, University of Liverpool, Liverpool L69 7ZD, UK
M. CAMPANER
Affiliation:
Department of Parasitology, Institute of Biomedical Science, University of São Paulo, São Paulo, SP, 05508-900, Brazil
A. C. V. JUNQUEIRA
Affiliation:
Department of Tropical Medicine, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, 21045-900, Brazil
J. R. COURA
Affiliation:
Department of Tropical Medicine, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, 21045-900, Brazil
N. AÑEZ
Affiliation:
Facultad de Ciencias, Departamento de Biologia, Universidad de Los Andes, Merida, 5101, Venezuela
J. J. SHAW
Affiliation:
Department of Parasitology, Institute of Biomedical Science, University of São Paulo, São Paulo, SP, 05508-900, Brazil
J. R. STEVENS
Affiliation:
School of Biological Sciences, University of Exeter, Exeter EX4 4PS, UK
M. M. G. TEIXEIRA
Affiliation:
Department of Parasitology, Institute of Biomedical Science, University of São Paulo, São Paulo, SP, 05508-900, Brazil
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Abstract

Phylogenetic relationships among Trypanosoma rangeli isolates from man, wild mammals and triatomine bugs from widespread geographical origin were inferred by comparison of the small subunit of ribosomal gene sequences. The phylogenetic trees indicated that the subgenus Herpetosoma is polyphyletic and strongly supported division of this group into two monophyletic lineages, one made up of T. rangeli, T. rangeli-like and allied species and other consisting of T. lewisi and related taxa. Based on phylogenetic analysis, morphology, behaviour in vertebrate and invertebrate hosts and epidemiology we propose: a) the validation of Herpetosoma as a taxon comprised only for species of group lewisi and the maintenance of T. lewisi as the type-species of this subgenus; b) the classification of T. rangeli, T. rangeli-like and allied species into a ‘T. rangeli-clade’ more closely related to Schizotrypanum than to T. lewisi or T. brucei. The phylogenetic tree disclosed at least 4 groups within the clade T. rangeli, all confirmed by polymorphism of the internal transcribed spacer, thus conferring for the first time phylogenetic support to groups of T. rangeli and corroborating the high complexity of this taxon. Grouping was independent of their mammalian host-species and geographical origin, indicating that other factors are determining this segregation.

Keywords

Trypanosoma rangeliHerpetosomaphylogenytaxonomySouth American trypanosomesBrazilian AmazonpolymorphismTrypanosoma lewisi
Type
Research Article
Information
Parasitology , Volume 129 , Issue 5 , November 2004 , pp. 549 - 561
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

AMORIM, M. I., MOMEN, H. & TRAUB-CSEKO, Y. M. ( 1993). Trypanosoma rangeli: sequence analysis of β-tubulin gene suggests closer relationship to Trypanosoma brucei than to Trypanosoma cruzi. Acta Tropica 53, 99–105.CrossRefGoogle Scholar
AÑEZ, N. ( 1981). Studies on Trypanosoma rangeli Tejera, 1920, 1. Deposition, migration and growth of T. rangeli in two mammals. In Parasitological Topics. Special Publication of the Society of Protozoologists, pp. 19–25. Allan Press, Kansas.
AÑEZ, N. ( 1982). Studies on Trypanosoma rangeli Tejera, 1920. IV – A reconsideration of its systematic position. Memórias do Instituto Oswaldo Cruz 77, 405–415.CrossRefGoogle Scholar
AÑEZ, N. ( 1983 a). Studies on Trypanosoma rangeli Tejera, 1920. VI – Developmental pattern in the haemolymph of Rhodnius prolixus. Memórias do Instituto Oswaldo Cruz 78, 413–419.Google Scholar
AÑEZ, N. ( 1983 b). Studies on Trypanosoma rangeli Tejera, 1920. V – Developmental pattern in the alimentary canal of Rhodnius prolixus. Memórias do Instituto Oswaldo Cruz 78, 183–191.Google Scholar
AÑEZ, N. ( 1984). Studies on Trypanosoma rangeli Tejera, 1920. VII – Its effect on the survival of infected triatomine bugs. Memórias do Instituto Oswaldo Cruz 79, 249–255.CrossRefGoogle Scholar
BURGDORFER, W., SCHIMIDT, M. L. & HOOGSTRAAL, H. ( 1973). Detection of Trypanosoma theileri in ethiopian cattle ticks. Acta Tropica 4, 340–346.Google Scholar
COURA, J. R., FERNANDES, O., ABOLEDA, M., BARETT, T. V., CARRARA, N., DEGRAVE, W. & CAMPBELL, D. A. ( 1996). Human infection by Trypanosoma rangeli in the Brazilian Amazon. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 278–279.CrossRefGoogle Scholar
CUPOLILLO, E., GRIMALDI, G. Jr., MOMEN, H. & BEVERLEY, S. M. ( 1995). Intergenic region typing (IRT): A rapid molecular approach to the characterization and evolution of Leishmania. Molecular and Biochemical Parasitology 73, 145–155.CrossRefGoogle Scholar
D'ALESSANDRO, A. & SARAIVA, N. G. ( 1992). Trypanosoma rangeli. In Parasitic Protozoa ( ed. Kreier, J. & Baker, J. R.), pp. 1–54. Academic Press, New York.
D'ALESSANDRO, A. & SARAIVA, N. G. ( 1999). Trypanosoma rangeli. In Protozoal Diseases ( ed. Gilles, H. M.), pp. 398–412. Edward Arnold, London.
DEANE, L. M., ALMEIDA, F. B., NETO, J. A. F. & SILVA, J. E. DA. ( 1972). Trypanosoma cruzi e outros tripanossomas em primatas brasileiros. Revista da Sociedade Brasileira de Medicina Tropical 6, 361.Google Scholar
EGER-MANGRICH, I., DE OLIVEIRA, M. A., GRISARD, E. C., DE SOUZA, W. & STEINDEL, M. ( 2001). Interaction of Trypanosoma rangeli Tejera, 1920 with different cell lines in vitro. Parasitology Research 87, 505–509.CrossRefGoogle Scholar
GOMES, S. A. O., FEDER, D., THOMAS, N. E. S., GARCIA, E. S. & AZAMBUJA, P. ( 1999). Rhodnius prolixus infected with Trypanosoma rangeli: In vivo and in vitro experiments. Journal of Invertebrate Pathology 73, 289–293.CrossRefGoogle Scholar
GRISARD, E. C., CAMPBELL, D. A. & ROMANHA, A. J. ( 1999). Mini-exon gene sequence polymorphism among Trypanosoma rangeli isolated from distinct geographical regions. Parasitology 118, 375–382.CrossRefGoogle Scholar
HAAG, J., O'H UIGIN, C. & OVERATH, P. ( 1998). The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 37–49.CrossRefGoogle Scholar
HANNAERT, V., OPPERDOES, F. R. & MICHELS, P. A. ( 1998). Comparison and evolutionary analysis of the glycosomal glyceraldehyde-3-phosphate dehydrogenase from different Kinetoplastida. Journal of Molecular Evolution 47, 728–738.CrossRefGoogle Scholar
HECKER, H., SCHWARZENBACH, M. & RUDIN, W. ( 1990). Development and interactions of Trypanosoma rangeli in and with the reduviid bug Rhodnius prolixus. Parasitology Research 76, 311–318.CrossRefGoogle Scholar
HENRIKSSON, J., SOLARI, A., RYDAKER, M., SOUSA, O. E. & PETTERSSON, U. ( 1996). Karyotype variability in Trypanosoma rangeli. Parasitology 112, 385–391.CrossRefGoogle Scholar
HOARE, C. A. ( 1964). Morphological and taxonomic studies on mammalian trypanosomes. X. Revision of the Systematics. Journal of Protozoology 11, 200–207.Google Scholar
HOARE, C. A. ( 1972). The Trypanosomes of Mammals. Blackwell, Oxford.
MACEDO, A. M., VALLEJO, G. A., CHIARI, E. & PENA, S. D. ( 1993). DNA fingerprinting reveals relationships between strains of Trypanosoma rangeli and Trypanosoma cruzi. EXS 67, 321–329.CrossRefGoogle Scholar
MACHADO, P. E., EGER-MANGRICH, I., ROSA, G., KOERICH, L. B., GRISARD, E. C. & STEINDEL, M. ( 2001). Differential susceptibility of triatomines of the genus Rhodnius to Trypanosoma rangeli strains from different geographical origins. International Journal for Parasitology 31, 632–634.CrossRefGoogle Scholar
MAIA DA SILVA, F., RODRIGUES, A. C., CAMPANER, M., TAKATA, C. S. A., BRIGIDO, M. C., JUNQUEIRA, A. C. V., COURA, J. R., TAKEDA, G. F., SHAW, J. J. & TEIXEIRA, M. M. G. ( 2004). Randomly amplified polymorphic DNA analysis of Trypanosoma rangeli and allied species from human, monkeys and other sylvatic mammals of Brazilian Amazon disclosed a new group and a species-specific marker. Parasitology 128, 283–294.CrossRefGoogle Scholar
MILES, M. A., ARIAS, J. R., VALENTE, S. A. S., NAIFF, R. D., DE SOUZA, A. A., POVOA, M. M., LIMA, J. A. N. & CEDILLOS, R. A. ( 1983). Vertebrate hosts and vectors of Trypanosoma rangeli in the Amazon basin of Brazil. American Journal of Tropical Medicine and Hygiene 32, 1251–1259.CrossRefGoogle Scholar
MOLYNEUX, D. ( 1976). Biology of the trypanosomes of the subgenus Herpetosoma. In Biology of the Kinetoplastida ( ed. Lumsden, W. H. R. & Evans, D. A.), pp. 285–325. Academic Press, London.
POSADA, D. & CRANDALL, K. A. ( 1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle Scholar
RAMIREZ, L. E., MACHADO, M. I., MAYWALD, P. G., MATOS, A., CHIARI, E. & SILVA, E. L. ( 1998). Primeira evidência de Trypanosoma rangeli no sudeste do Brasil, região endêmica para doença de Chagas. Revista da Sociedade Brasileira de Medicina Tropical 31, 99–102.CrossRefGoogle Scholar
SAITOU, N. & NEI, M. ( 1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
SHAW, J. J. ( 1985). The hemoflagellates of sloths, vermilinguas (anteaters), and armadillos. In The Evolution and Ecology of Armadillos, Sloths and Vermilingues ( ed. Montegomery, G. G.), pp. 279–292. Smithsonian Institute Press, Washington DC.
SILVA, F. M., RODRIGUES, A. C., CAMPANER, M., FERREIRA, R. C., TAKEDA, G. F. & TEIXEIRA, M. M. G. ( 1999). Trypanosoma (Herpetosoma) spp.: genetic diversity and taxonomic position defined by ribosomal, spliced leader and RAPD markers. Memórias do Instituto Oswaldo Cruz 94 (Suppl. II), 158.Google Scholar
SOUSA, O. E. & DAWSON, G. A. ( 1976). Trypanosome infections in the marmoset (Saguinus geoffroyi) from the Panama Canal Zone. American Journal of Tropical Medicine and Hygiene 25, 407–409.CrossRefGoogle Scholar
STEINDEL, M., CARVALHO PINTO, J. C., TOMA, H. K., MANGIA, R. H. R., RIBEIRO-RODRIGUES, R. & ROMANHA, A. J. ( 1991). Trypanosoma rangeli (Tejera, 1920) isolated from sylvatic rodent (Echimys dasytrix) in Santa Catarina island, Santa Catarina state: first report of this trypanosome in Southern Brazil. Memórias do Instituto Oswaldo Cruz 86, 73–79.CrossRefGoogle Scholar
STEINDEL, M., DIAS NETO, E., PINTO, C. J., GRISARD, E. C., MENEZES, C. L., MURTA, S. M., SIMPSON, A. J. & ROMANHA, A. J. ( 1994). Randomly amplified polymorphic DNA (RAPD) and isoenzyme analysis of Trypanosoma rangeli strains. Journal of Eukaryotic Microbiology 41, 261–267.CrossRefGoogle Scholar
STEVENS, J. R., NOYES, H. A., DOVER, G. A. & GIBSON, W. C. ( 1999 b). The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.Google Scholar
STEVENS, J. R., NOYES, H. A., SCHOFIELD, C. J. & GIBSON, W. ( 2001). The molecular evolution of Trypanosomatidae. Advances in Parasitology 48, 1–56.CrossRefGoogle Scholar
STEVENS, J. R. & GIBSON, W. ( 1999). The molecular evolution of trypanosomes. Parasitology Today 15, 432–437.CrossRefGoogle Scholar
STEVENS, J. R., TEIXEIRA, M. M. G., BINGLE, L. E. & GIBSON, W. C. ( 1999 a). The taxonomic position and evolutionary relationships of Trypanosoma rangeli. International Journal for Parasitology 29, 749–757.Google Scholar
STRIMMER, K. N. & VON HAESELER, A. ( 1996). Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13, 964–969.CrossRefGoogle Scholar
TANAKA, T., KANEDA, Y., LIDA, A. & TANAKA, M. ( 1994). Homologous cysteine proteinase genes located on two different chromosomes from Trypanosoma rangeli. International Journal for Parasitology 24, 179–188.CrossRefGoogle Scholar
TOBIE, E. J. ( 1964). Increased infectivity of a cyclically maintained strain of Trypanosoma rangeli to Rhodnius prolixus and mode of transmission by invertebrate host. Journal of Parasitology 50, 593–598.CrossRefGoogle Scholar
TOBIE, E. J. ( 1970). Observations on the development of Trypanosoma rangeli in the haemocoele of Rhodnius prolixus. Journal of Invertebrate Pathology 15, 118–125.CrossRefGoogle Scholar
VALLEJO, G. A., GUHL, F., CARRANZA, J. C., MORENO, J., TRIANA, O. & GRISARD, E. C. ( 2003). Parity between kinetoplast DNA and mini-exon gene sequences supports either clonal evolution or speciation in Trypanosoma rangeli strains isolated from Rhodnius colombiensis, R. pallescens and R. prolixus in Colombia. Infection, Genetics and Evolution 3, 39–45.CrossRefGoogle Scholar
VARGAS, N., SOUTO, R. P., CARRANZA, J. C., VALLEJO, G. A. & ZINGALES, B. ( 2000). Amplification of a specific repetitive DNA sequence for Trypanosoma rangeli identification and its potential application in epidemiological investigations. Experimental Parasitology 96, 147–159.CrossRefGoogle Scholar
ZICCARDI, M., OLIVEIRA, R. L., LAINSON, R., BRÍGIDO, M. C. O. & MUNIZ, J. A. P. C. ( 2000). Trypanosomes of non-human primates from the national center of primates, Ananindeua, State of Pará, Brazil. Memórias do Instituto Oswaldo Cruz 95, 157–159.CrossRefGoogle Scholar