Hostname: page-component-6dbcb7884d-xl9kw Total loading time: 0 Render date: 2025-02-14T07:52:27.246Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of spliced leader genes of Trypanosoma (Megatrypanum) theileri: phylogeographical analysis of Brazilian isolates from cattle supports spatial clustering of genotypes and parity with ribosomal markers

Published online by Cambridge University Press:  21 September 2009

A. C. RODRIGUES ,
H. A. GARCIA ,
J. S. BATISTA ,
A. H. H. MINERVINO ,
G. GÓES-CAVALCANTE ,
F. MAIA DA SILVA ,
R. C. FERREIRA ,
M. CAMPANER ,
F. PAIVA  and
M. M. G. TEIXEIRA
A. C. RODRIGUES
Affiliation:
Departamento de Parasitologia, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
H. A. GARCIA
Affiliation:
Departamento de Parasitologia, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
J. S. BATISTA
Affiliation:
Departamento de Ciências Animais, Laboratório de Patologia Veterinária, Universidade Federal Rural do Semi-Árido, RN, 59625-900, Brasil
A. H. H. MINERVINO
Affiliation:
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, SP, 05508-900, Brasil
G. GÓES-CAVALCANTE
Affiliation:
Central de Diagnóstico Veterinário, Universidade Federal do Pará, PA, 66080-000, Brasil
F. MAIA DA SILVA
Affiliation:
Departamento de Parasitologia, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
R. C. FERREIRA
Affiliation:
Departamento de Parasitologia, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
M. CAMPANER
Affiliation:
Departamento de Parasitologia, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
F. PAIVA
Affiliation:
Departamento de Parasitologia Veterinária, Universidade Federal do Mato Grosso do Sul, MS, 79070-900, Brasil
M. M. G. TEIXEIRA*
Affiliation:
Departamento de Parasitologia, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
*
*Corresponding author: Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil. Tel: +55 11 3091 7268. Fax: +55 11 3091 7417. E-mail: mmgteix@icb.usp.br
Get access Rights & Permissions [Opens in a new window]

Summary

Trypanosoma (Megatrypanum) theileri from cattle and trypanosomes of other artiodactyls form a clade of closely related species in analyses using ribosomal sequences. Analysis of polymorphic sequences of a larger number of trypanosomes from broader geographical origins is required to evaluate the clustering of isolates as suggested by previous studies. Here, we determined the sequences of the spliced leader (SL) genes of 21 isolates from cattle and 2 from water buffalo from distant regions of Brazil. Analysis of SL gene repeats revealed that the 5S rRNA gene is inserted within the intergenic region. Phylogeographical patterns inferred using SL sequences showed at least 5 major genotypes of T. theileri distributed in 2 strongly divergent lineages. Lineage TthI comprises genotypes IA and IB from buffalo and cattle, respectively, from the Southeast and Central regions, whereas genotype IC is restricted to cattle from the Southern region. Lineage TthII includes cattle genotypes IIA, which is restricted to the North and Northeast, and IIB, found in the Centre, West, North and Northeast. PCR-RFLP of SL genes revealed valuable markers for genotyping T. theileri. The results of this study emphasize the genetic complexity and corroborate the geographical structuring of T. theileri genotypes found in cattle.

Keywords

Trypanosoma theilerispliced leader geneITS rDNAphylogenyevolutionphylogeographybovidspopulational structure
Type
Research Article
Information
Parasitology , Volume 137 , Issue 1 , January 2010 , pp. 111 - 122
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

Aksoy, S., Shay, G. L., Villanueva, M. S., Beard, C. B. and Richards, F. F. (1992). Spliced leader RNA sequences of Trypanosoma rangeli are organized within the 5S rRNA-encoding genes. Gene 113, 239–243.CrossRefGoogle ScholarPubMed
Bose, R. and Heister, N. C. (1993). Development of Trypanosoma (Megatrypanum) theileri in tabanids. The Journal of Eukaryotic Microbiology 40, 788–792. doi:10.1111/j.1550-7408.1993.tb04475.x.CrossRefGoogle ScholarPubMed
Bose, R., Petersen, K., Pospichal, H., Buchanan, N. and Tait, A. (1993). Characterization of Megatrypanum trypanosomes from European Cervidae. Parasitology 107, 55–61. doi:10.1017/S0031182000079403.CrossRefGoogle ScholarPubMed
Bose, R., Friedhoff, K. T., Olbrich, S., Büscher, G. and Domeyer, I. (1987). Transmission of Trypanosoma theileri to cattle by Tabanidae. Parasitology Research 73, 421–424.CrossRefGoogle ScholarPubMed
Brisse, S., Verhoef, J. and Tibayrenc, M. (2001). Characterisation of large and small subunit rRNA and mini-exon genes further supports the distinction of six Trypanosoma cruzi lineages. International Journal for Parasitology 31, 1218–1226. doi:10.1016/S0020-7519(01)00238-7.CrossRefGoogle ScholarPubMed
Cortez, A. P., Ventura, R. M., Rodrigues, A. C., Batista, J. S., Paiva, F., Añez, 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. doi:10.1017/S0031182006000254.CrossRefGoogle ScholarPubMed
Dirie, M. F., Bornstein, S., Wallbanks, K. R., Stiles, J. K. and Molyneux, D. H. (1990). Zymogram and life-history studies on trypanosomes of the subgenus Megatrypanum. Parasitology Research 76, 669–674.CrossRefGoogle ScholarPubMed
Doherty, M. L., Windle, H., Voorheis, H. P., Larkin, H., Casey, M., Clery, D. and Murray, M. (1993). Clinical disease associated with Trypanosoma theileri infections in a calf in Ireland. Veterinary Record 26, 653–656.CrossRefGoogle Scholar
Drouin, G. and de Sá, M. M. (1995). The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. Molecular Biology and Evolution 12, 481–493.Google Scholar
Falla, A., Herrera, C., Fajardo, A., Montilla, M., Vallejo, G. A. and Guhl, F. (2009). Haplotype identification within Trypanosoma cruzi I in Colombian isolates from several reservoirs, vectors and humans. Acta Tropica 110, 15–21. doi:10.1016/j.actatropica.2008.12.003.CrossRefGoogle ScholarPubMed
Fernandes, O., Santos, S. S., Cupolillo, E., Mendonça, M. B. A., Junqueira, A., Santos, L. C., Derré, R., Sturm, N. R., Naiff, R. D., Barrett, T. V., Campbell, D. A. and Coura, J. R. (2001). A mini-exon multiplex polymerase chain reaction to distinguish the major groups of Trypanosoma cruzi and T. rangeli in the Brazilian Amazon. Transactions of the Royal Society of Hygiene and Tropical Medicine 95, 97–99.CrossRefGoogle Scholar
Fernandes, O., Teixeira, M. M. G., Sturm, N. R., Sousa, M. A., Camargo, E. P., Degrave, W. M. and Campbell, D. A. (1997). Mini-exon gene sequence define six groups within the genus Crithidia. The Journal of Eukaryotic Microbiology 44, 535–539.CrossRefGoogle ScholarPubMed
Ferreira, R. C., de Souza, A. A., Freitas, R. A., Campaner, M., Takata, C. S. A., Barrett, T. V., Shaw, J. J. and Teixeira, M. M. G. (2007). A Phylogenetic lineage of closely related trypanosomes (Trypanosomatidae, Kinetoplastida) of anurans and sand flies (Psychodidae, Diptera) sharing the same ecotopes in Brazilian Amazonia. The Journal of Eukaryotic Microbiology 55, 427–435. doi:10.1111/j.1550-7408.2008.00342.x.CrossRefGoogle Scholar
Gibson, W., Bingle, L., Blendeman, W., Brown, J., Wood, J. and Stevens, J. (2000). Structure and sequence variation of the trypanosome spliced leader transcript. Molecular and Biochemical Parasitology 107, 269–277. doi:10.1016/S0166-6851(00)00193-6.CrossRefGoogle ScholarPubMed
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. doi:10.1016/j.meegid.2008.10.011.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. doi:10.1016/j.ympev.2007.03.023.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. doi:10.1016/j.ijpara.2004.12.005.CrossRefGoogle ScholarPubMed
Hatama, S., Shibahara, T., Suzuki, M., Kadota, K., Uchida, I. and Kanno, T. (2007). Isolation of a Megatrypanum trypanosome from sika deer (Cervus nippon yesoensis) in Japan. Veterinary Parasitology 149, 56–64. doi:10.1016/j.vetpar.2007.07.019.CrossRefGoogle ScholarPubMed
Heiman, M. (1997). Webcutter 2.0. (http://rna.lundberg.gu.se/cutter2/).Google Scholar
Herrera, C., Bargues, M. D., Fajardo, A., Montilla, M., Triana, O., Vallejo, G. A. and Guhl, F. (2007). Identifying four Trypanosoma cruzi I isolate haplotypes from different geographic regions in Colombia. Infection Genetic and Evolution 7, 535–539. doi:10.1016/j.meegid.2006.12.003.CrossRefGoogle ScholarPubMed
Hoare, C. A. (1972). Subgenus Megatrypanum. In The Trypanosomes of Mammals: A Zoological Monograph (ed. Hoare, C. A.), pp. 123–141. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Maia Da Silva, F., Junqueira, A. C., Campaner, M., Rodrigues, A. C., Crisante, G., Ramirez, L. E., Caballero, Z. C., Monteiro, F. A., Coura, J. R., Añez, N. and Teixeira, M. M. G. (2007). Comparative phylogeography of Trypanosoma rangeli and Rhodnius (Hemiptera: Reduviidae) supports a long coexistence of parasite lineages and their sympatric vectors. Molecular Ecology 16, 3361–3373. doi:10.1111/j.1365-294X.2007.03371.x.CrossRefGoogle ScholarPubMed
Maia da Silva, F., Marcili, A., Lima, L., Cavazzana, M Jr., Ortiz, P. A., Campaner, M., Takeda, G. F., Paiva, F., Nunes, V. L., Camargo, E. P. and Teixeira, M. M. G. (2009). Trypanosoma rangeli isolates of bats from Central Brazil: genotyping and phylogenetic analysis enable description of a new lineage using spliced-leader gene sequences. Acta Tropica 109, 199–207. doi:10.1016/j.actatropica.2008.11.005.CrossRefGoogle ScholarPubMed
Maslov, D. A., Westenberger, S. J., Xu, X., Campbell, D. A. and Sturm, N. R. (2007). Discovery and barcoding by analysis of splice leader RNA gene sequences of new isolates of Trypanosomatidae from Heteroptera in Costa Rica and Ecuador. The Journal of Eukaryotic Microbiology 54, 57–65. doi:10.1111/j.1550-7408.2006.00150.x.CrossRefGoogle ScholarPubMed
Matzura, O. and Wennborg, A. (1996). RNAdraw: an Integrated Program for RNA Secondary Structure Calculation and Analysis under 32-bit Microsoft Windows.Google ScholarPubMed
Mejía-Jaramillo, A. M., Arboleda-Sánchez, S., Rodríguez, I. B., Cura, C., Salazar, A., del Mazo, J., Triana-Chávez, O. and Schijman, A. G. (2009). Geographical clustering of Trypanosoma cruzi I groups from Colombia revealed by low-stringency single specific primer-PCR of the intergenic regions of spliced-leader genes. Parasitology Research 104, 399–410. doi 10.1007/s00436-008-1212-0.CrossRefGoogle ScholarPubMed
O'Connor, O., Bosseno, M-F., Barnabé, C., Douzery, E. J. P. and Brenière, S. F. (2007). Genetic clustering of Trypanosoma cruzi I lineage evidenced by intergenic miniexon gene sequencing. Infection, Genetics and Evolution 7, 587–593. doi:10.1016/j.meegid.2007.05.003.CrossRefGoogle ScholarPubMed
Podlipaev, S. A., Sturm, N. R., Fiala, I., Fernandes, O., Westenberger, S. J., Dollet, M., Campbell, D. A. and Lukes, J. (2004). Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. The Journal of Eukaryotic Microbiology 51, 283–290. doi:10.1111/j.1550-7408.2004.tb00568.x.CrossRefGoogle ScholarPubMed
Roditi, I. (1992). Trypanosoma vivax: linkage of mini-exon (spliced leader) and 5S ribosomal RNA genes. Nucleic Acids Research 20, 1995.CrossRefGoogle ScholarPubMed
Rodrigues, A. C., Paiva, F., Campaner, M., Stevens, J. R., Noyes, H. A. and Teixeira, M. M. G. (2006). Phylogeny of Trypanosoma (Megatrypanum) theileri and related trypanosomes reveals lineages of isolates associated with artiodactyl hosts diverging on SSU and ITS ribosomal sequences. Parasitology 132, 215–224. doi:10.1017/S0031182005008929.CrossRefGoogle ScholarPubMed
Rodrigues, A., Campaner, M., Takata, C. S., Dell' Porto, A., Milder, R. V., Takeda, G. F. and Teixeira, M. M. G. (2003). Brazilian isolates of Trypanosoma (Megatrypanum) theileri: diagnosis and differentiation of isolates from cattle and water buffalo based on biological characteristics and randomly amplified DNA sequences. Veterinary Parasitology 116, 185–207. doi:10.1016/S0304-4017(03)00236-X.CrossRefGoogle ScholarPubMed
Schafler, D. H. (1979). Trypanosoma theileri: a literature review and report of incidence in New York cattle. Cornell Veterinarian 69, 411–425.Google Scholar
Seifi, H. A. (1995). Clinical trypanosomosis due to Trypanosoma theileri in a cow in Iran. Tropical Animal Health and Production 27, 93–94.CrossRefGoogle Scholar
Serrano, M. G., Nunes, L. R., Campaner, M., Buck, G. A., Camargo, E. P. and Teixeira, M. M. G. (1999 a). Trypanosomatidae: Phytomonas detection in plants and phytophagous insects by PCR amplification of a genus-specific sequence of the spliced leader gene. Experimental Parasitology 91, 268–279. doi:10.1006/expr.1998.4379.CrossRefGoogle ScholarPubMed
Serrano, M. G., Campaner, M., Buck, G. A., Teixeira, M. M. G. and Camargo, E. P. (1999 b). PCR amplification of the spliced leader gene for the diagnosis of Trypanosomatid parasites of plants and insects in methanol-fixed smears. FEMS Microbiology Letters 176, 241–246.CrossRefGoogle ScholarPubMed
Souto, R. P., Fernandes, O., Macedo, A. M., Campbell, D. and Zingales, B. (1996). DNA marker define two major phylogenetic lineages of Trypanosoma cruzi. Molecular and Biochemical Parasitology 83, 141–152. doi:10.1016/S0166-6851(96)02755-7.CrossRefGoogle ScholarPubMed
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690. doi:10.1093/bioinformatics/btl446.CrossRefGoogle ScholarPubMed
Stevens, J. R., Teixeira, M. M. G., Bingle, L. E. and Gibson, W. C. (1999). The taxonomic position and evolutionary relationships of Trypanosoma rangeli. International Journal for Parasitology 29, 749–757. doi:10.1016/S0020-7519(99)00016-8.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002). PAUP* Phylogenetic Analysis using Parsimony (*and other Methods) Version 4.0b10. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Thomas, S., Westenberger, S. J., Campbell, D. A. and Sturm, N. R. (2005). Intragenomic spliced leader RNA array analysis of kinetoplastids reveals unexpected transcribed region diversity in Trypanosoma cruzi. Gene 352, 100–108. doi:10.1016/j.gene.2005.04.002.CrossRefGoogle ScholarPubMed
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Urrea, D. A., Carranza, J. C., Cuba, C. A., Gurgel-Gonçalves, R., Guhl, F., Schofield, C. J., Triana, O. and Vallejo, G. A. (2005). Molecular characterisation of Trypanosoma rangeli strains isolated from Rhodnius ecuadoriensis in Peru, R. colombiensis in Colombia and R. pallescens in Panama, supports a co-evolutionary association between parasites and vectors. Infection Genetic and Evolution 5, 123–129. doi:10.1016/j.meegid.2004.07.005.CrossRefGoogle Scholar
Ventura, R. M., Paiva, F., Silva, R. M. S., Takeda, G. F., Buck, G. A. and Teixeira, M. M. G. (2001). Trypanosoma vivax: characterization of the spliced-leader gene of a Brazilian stock and species-specific detection by PCR amplification of an intergenic spacer sequence. Experimental Parasitology 99, 37–48. doi:10.1006/expr.2001.4641.CrossRefGoogle ScholarPubMed
Wells, E. A. (1976). Subgenus Megatrypanum. In Biology of the Kinetoplastida (ed. Lumsden, W. H. R. and Evans, D. A.), pp. 257–275. Academic Press, London, UK.Google Scholar
Westenberger, S. J., Sturm, N. R. and Campbell, D. A. (2006). Trypanosoma cruzi 5S rRNA arrays define five groups and indicate the geographic origins of an ancestor of the heterozygous hybrids. International Journal for Parasitology 36, 337–346. doi:10.1016/j.ijpara.2005.11.002.CrossRefGoogle ScholarPubMed
Westenberger, S. J., Sturm, N. R., Yanega, D., Podlipaev, S. A., Zeledón, R., Campbell, D. A. and Maslov, D. A. (2004). Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the spliced leader RNA gene. Parasitology 129, 537–547. doi: 10.1017/S003118200400592X.CrossRefGoogle ScholarPubMed