1887

Abstract

Three strains of a trypanosomatid protozoan were isolated from the midguts of two naturally infected species of biting midges [ () and () ] and characterized by light and electron microscopy and by molecular techniques. Morphological characteristics and sequences of the 18S rRNA, 5S rRNA, spliced leader RNA and glycosomal glyceraldehyde-3-phosphate dehydrogenase genes indicate that the studied flagellates represent a novel phylogenetic lineage within the Trypanosomatidae. Based on phylogenetic analyses, the novel endosymbiont-free, monoxenous trypanosomatid was classified as gen. nov., sp. nov. Interestingly, it is closely related to another trypanosomatid species that parasitizes the sand fly , a blood-sucking dipteran from South America. The type strain of sp. nov., ICUL/CZ/2000/CER3, was obtained from Malpighian tubes. Of 2518 females of seven species of biting midges trapped in the Czech Republic, more than 1.5 % were infected by trypanosomatid parasites. An unrelated insect species, () , was experimentally infected with , demonstrating that its host range extends to different subgenera of biting midges.

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2007-02-01
2019-10-18
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References

  1. Abreu Filho, B. A., Dias Filho, B. P., Vermelho, A. B., Jankevicius, S. I., Jankevicius, J. V. & dos Santos, R. L. ( 2001; ). Surface component characterization as taxonomic tools for Phytomonas spp. identification. Parasitol Res 87, 138–144.[CrossRef]
    [Google Scholar]
  2. Bastin, P., Pullen, T. J., Moreira-Leite, F. F. & Gull, K. ( 2000; ). Inside and outside of the trypanosome flagellum: a multifunctional organelle. Microbes Infect 2, 1865–1874.[CrossRef]
    [Google Scholar]
  3. d'Ávila-Levy, C. M., Araújo, F. M., Vermelho, A. B., Branquinha, M. H., Alviano, C. S., Soares, R. M. A. & dos Santos, A. L. S. ( 2004; ). Differential lectin recognition of glycoproteins in choanomastigote-shaped trypanosomatids: taxonomic implications. FEMS Microbiol Lett 231, 171–176.[CrossRef]
    [Google Scholar]
  4. Dollet, M., Sturm, N. R., Sanchéz-Moreno, M. & Campbell, D. A. ( 2000; ). 5S ribosomal RNA gene repeat sequences define at least eight groups of plant trypanosomatids (Phytomonas spp.): phloem-restricted pathogens form a distinct section. J Eukaryot Microbiol 47, 569–574.[CrossRef]
    [Google Scholar]
  5. Fernandes, O., Teixeira, M. M. G., Sturm, N. R., Sousa, M. A., Camargo, E. P., Degrave, W. M. & Campbell, D. A. ( 1997; ). Mini-exon gene sequences define six groups within the genus Crithidia. J Eukaryot Microbiol 44, 535–539.
    [Google Scholar]
  6. Fernandes, O., Santos, S. S., Cupolillo, E., Mendonca, B., Derre, R., Junqueira, A. C. V., Santos, L. C., Sturm, N. R., Naiff, R. D. & other authors ( 2001; ). A mini-exon multiplex polymerase chain reaction to distinguish the major groups of Trypanosoma cruzi and T. rangeli in the Brazilian Amazon. Trans R Soc Trop Med Hyg 95, 97–99.[CrossRef]
    [Google Scholar]
  7. Gadelha, C., Wickstead, B., de Souza, W., Gull, K. & Cunha-e-Silva, N. ( 2005; ). Cryptic paraflagellar rod in endosymbiont-containing kinetoplastid protozoa. Eukaryot Cell 4, 516–525.[CrossRef]
    [Google Scholar]
  8. Guindon, S. & Gascuel, O. ( 2003; ). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.[CrossRef]
    [Google Scholar]
  9. Hamilton, P. B., Stevens, J. R., Gaunt, M. W., Gidley, J. & Gibson, W. C. ( 2004; ). Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. Int J Parasitol 34, 1393–1404.[CrossRef]
    [Google Scholar]
  10. Hoare, C. A. & Wallace, F. G. ( 1966; ). Developmental stages of trypanosomatid flagellates: a new terminology. Nature 212, 1385–1386.[CrossRef]
    [Google Scholar]
  11. Hollar, L., Lukeš, J. & Maslov, D. A. ( 1998; ). Monophyly of endosymbiont containing trypanosomatids: phylogeny versus taxonomy. J Eukaryot Microbiol 45, 293–297.[CrossRef]
    [Google Scholar]
  12. Jiménez, M. I., López-Vélez, R., Molina, R., Cañavate, C. & Alvar, J. ( 1996; ). HIV-coinfection with a currently non-pathogenic flagellate. Lancet 347, 264–265.
    [Google Scholar]
  13. Lukeš, J. & Votýpka, J. ( 2000; ). Trypanosoma avium: novel features of the kinetoplast structure. Exp Parasitol 96, 178–181.[CrossRef]
    [Google Scholar]
  14. Lukeš, J., Jirků, M., Doležel, D., Král'ová, I., Hollar, L. & Maslov, D. A. ( 1997; ). Analysis of ribosomal RNA genes suggests that trypanosomes are monophyletic. J Mol Evol 44, 521–527.[CrossRef]
    [Google Scholar]
  15. Merzlyak, E., Yurchenko, V., Kolesnikov, A. A., Alexandrov, K., Podlipaev, S. A. & Maslov, D. A. ( 2001; ). Diversity and phylogeny of insect trypanosomatids based on small subunit rDNA genes: polyphyly of Leptomonas and Blastocrithidia. J Eukaryot Microbiol 48, 161–169.[CrossRef]
    [Google Scholar]
  16. Miranda, K., Docampo, R., Grillo, O. & de Souza, W. ( 2004; ). Acidocalcisomes of trypanosomatids have species-specific elemental composition. Protist 155, 395–405.[CrossRef]
    [Google Scholar]
  17. Momen, H. ( 2001; ). Some current problems in the systematics of Trypanosomatids. Int J Parasitol 31, 640–642.[CrossRef]
    [Google Scholar]
  18. Podlipaev, S. A. ( 1990; ). Catalogue of world fauna of Trypanosomatidae (Protozoa). Proc Zool Inst Leningrad 144, 1–178.
    [Google Scholar]
  19. Podlipaev, S. A. ( 2000; ). Insect trypanosomatids: the need to know more. Mem I Oswaldo Cruz 95, 517–522.[CrossRef]
    [Google Scholar]
  20. Podlipaev, S. A., Sturm, N. R., Fiala, I., Fernandes, O., Westenberger, S. J., Dollet, M., Campbell, D. A. & Lukeš, J. ( 2004a; ). Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. J Eukaryot Microbiol 51, 283–290.[CrossRef]
    [Google Scholar]
  21. Podlipaev, S. A., Votýpka, J., Jirků, M., Svobodová, M. & Lukeš, J. ( 2004b; ). Herpetomonas ztiplika n. sp. (Kinetoplastida: Trypanosomatidae): a parasite of the blood-sucking biting midge Culicoides kibunensis Tokunaga, 1937 (Diptera: Ceratopogonidae). J Parasitol 90, 342–347.[CrossRef]
    [Google Scholar]
  22. Poinar, G., Jr, & Poinar, R. ( 2004; ). Paleoleishmania proterus n. gen., n. sp., (Trypanosomatidae : Kinetoplastida) from Cretaceous Burmese amber. Protist 155, 305–310.[CrossRef]
    [Google Scholar]
  23. Poinar, G., Jr, & Poinar, R. ( 2005; ). Fossil evidence of insect pathogens. J Invertebr Pathol 89, 243–250.[CrossRef]
    [Google Scholar]
  24. Santos, D. O., Bourguignon, S. C., Castro, C. H., Silva, J. S., Franco, L. S., Hespanhol, R., Soares, M. J. & Corte-Real, S. ( 2004; ). Infection of mouse dermal fibroblasts by the monoxenous trypanosomatid protozoa Crithidia deanei and Herpetomonas roitmani. J Eukaryot Microbiol 51, 570–574.[CrossRef]
    [Google Scholar]
  25. Santos, A. L. S., Abreu, C. M., Alviano, C. S. & Soares, R. M. A. ( 2005; ). Use of proteolytic enzymes as an additional tool for trypanosomatid identification. Parasitology 130, 79–88.[CrossRef]
    [Google Scholar]
  26. Simpson, A. G. B., Lukeš, J. & Roger, A. J. ( 2002; ). The evolutionary history of kinetoplastids and their kinetoplasts. Mol Biol Evol 19, 2071–2083.[CrossRef]
    [Google Scholar]
  27. Simpson, A. G. B., Stevens, J. R. & Lukeš, J. ( 2006; ). The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22, 168–174.[CrossRef]
    [Google Scholar]
  28. Stevens, J. R. ( 2001; ). One million insects – a lot of parasites? Trends Parasitol 17, 119–120.
    [Google Scholar]
  29. Stevens, J. R., Noyes, H. A., Schofield, C. J. & Gibson, W. ( 2001; ). The molecular evolution of Trypanosomatidae. Adv Parasitol 48, 1–56.
    [Google Scholar]
  30. Swofford, D. L. ( 2001; ). paup*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA: Sinauer Associates.
  31. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  32. Vickerman, K. ( 1994; ). The evolutionary expansion of the trypanosomatid flagellates. Int J Parasitol 24, 1317–1331.[CrossRef]
    [Google Scholar]
  33. Votýpka, J., Oborník, M., Volf, P., Svobodová, M. & Lukeš, J. ( 2002; ). Trypanosoma avium of raptors (Falconiformes): phylogeny and identification of vectors. Parasitology 125, 253–263.
    [Google Scholar]
  34. Wallace, F. G. ( 1966; ). The trypanosomatid parasites of insects and arachnids. Exp Parasitol 18, 124–193.[CrossRef]
    [Google Scholar]
  35. Wallace, F. G., Camargo, E. P., McGhee, R. B. & Roitman, I. ( 1983; ). Guidelines for the description of new species of lower trypanosomatids. J Protozool 30, 308–313.[CrossRef]
    [Google Scholar]
  36. Westenberger, S. J., Sturm, N. R., Yanega, D., Podlipaev, S. A., Zeledón, R., Campbell, D. A. & Maslov, D. A. ( 2004; ). Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the spliced leader RNA gene. Parasitology 129, 537–547.[CrossRef]
    [Google Scholar]
  37. Yurchenko, V., Lukeš, J., Xu, X. & Maslov, D. A. ( 2006; ). An integrated morphological and molecular approach to a new species description in the Trypanosomatidae: the case of Leptomonas podlipaevi n. sp., a parasite of Boisea rubrolineata (Hemiptera: Rhopalidae). J Eukaryot Microbiol 53, 103–111.[CrossRef]
    [Google Scholar]
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GenBank accession numbers for the 18S, 5S and SL RNA and partial gGAPDH gene sequences analysed in this study and the composition of the final combined dataset. [PDF](53 KB)

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A representative RAPD gel and a phylogenetic tree inferred from the dataset of all the RAPD patterns. [PDF](99 KB)

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