Folia Parasitologica, vol. 61 (2014), issue 2

Folia Parasitologica 61[2] 97-112 (2014) | 10.14411/fp.2014.023

Ultrastructure and molecular phylogeny of four new species of monoxenous trypanosomatids from flies (Diptera: Brachycera) with redefinition of the genus Wallaceina

Vyacheslav Yurchenko1*, Jan Votýpka2,3*, Martina Tesařová3, Helena Klepetková2, Natalya Kraeva1, Milan Jirků3, Julius Lukeš3,4
1 Life Science Research Centre, University of Ostrava, Ostrava, Czech Republic;
2 Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic;
3 Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic;
4 Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic
* These authors contributed equally to this work This article contains supporting information (Fig. S1) online at http://folia.paru.cas.cz/suppl/2014-61-2-97.pdf

Four new species of monoxenous kinetoplastid parasites are described from Brachycera flies, namely Wallaceina raviniae Votýpka et Lukeš, 2014 and Crithidia otongatchiensis Votýpka et Lukeš, 2014 from Ecuador, Leptomonas moramango Votýpka et Lukeš, 2014 from Madagascar, and Crithidia pragensis Votýpka, Klepetková et Lukeš, 2014 from the Czech Republic. The new species are described here based on sequence analysis of their spliced leader (SL) RNA, glycosomal glyceraldehyde 3-phosphate dehydrogenase (gGAPDH) and small subunit (SSU) rRNA genes, as well as their morphology and ultrastructure. High-pressure freezing and Bernhard's EDTA regressive staining, used for the first time for monoxenous (one host) trypanosomatids, revealed the presence of viral particles with cytosolic localization in one and unique mitochondrial localization in another species. In accordance with previous observations, our results emphasize a discrepancy between morphology and molecular taxonomy of the family Trypanosomatidae. All four newly described species are represented by typical morphotypes (mainly choano- and promastigotes) and are virtually indistinguishable from other monoxenous trypanosomatids by morphology. Nevertheless, they all differ in their phylogenetic affinities. Whereas three of them grouped within the recently defined subfamily Leishmaniinae, which includes numerous representatives of the genera Leishmania Ross, 1903, Crithidia Léger, 1902 and Leptomonas Kent, 1880, the fourth species clusters together with the 'collosoma' clade (named after 'Leptomonas' collosoma Wallace, Clark, Dyer et Collins, 1960). Here we demonstrate that the 'collosoma' group represents the elusive genus Wallaceina Podlipaev, Frolov et Kolesnikov, 1999. We redefine this genus in molecular terms based on similarities of the respective molecular markers and propose to use this taxon name for the group of species of the 'collosoma' clade.

Keywords: Kinetoplastida, Trypanosomatidae, monoxenous kientoplastids, Leishmaniinae, molecular taxonomy, phylogeny

Received: September 1, 2013; Accepted: December 4, 2013; Prepublished online: January 27, 2014; Published: April 14, 2014


Attachments:

Download fileYurchenko_Supporting_information.pdf

File size: 2.79 MB

References

  1. Bernhard W. 1969: A new staining procedure for electron microscopical cytology. J. Ultrastruct. Res. 27: 250-265 Go to original source... Go to PubMed...
  2. Borghesan T.C., Ferreira R.C., Takata C.S., Campaner M., Borda C.C., Paiva F., Milder R.V., Teixeira M.M., Camargo E.P. 2013: Molecular phylogenetic redefinition of Herpetomonas (Kinetoplastea, Trypanosomatidae), a genus of insect parasites associated with flies. Protist 164: 129-152 Go to original source... Go to PubMed...
  3. Brun R. 1974: Ultrastructure and life cycle of Herpetomonas muscarum, "Herpetomonas mirabilis" and Crithidia luciliae in Chrysomyia chloropyga. Acta Trop. 32: 219-290 Go to PubMed...
  4. Bulat S.A., Mokrousov I.V., Podlipaev S.A. 1999: Classification of trypanosomatids from insects and plants by the UP-PCR (Universally Primed PCR) technique and cross dot blot hybridization of PCR products. Eur. J. Protistol. 35: 319-326 Go to original source... Go to PubMed...
  5. Flegontov P., Votypka J., Skalicky T., Logacheva M.D., Penin A.A., Tanifuji G., Onodera N.T., Kondrashov A.S., Volf P., Archibald J.M., Lukes J. 2013: Paratrypanosoma is a novel early-branching trypanosomatid. Curr. Biol. 23: 1787-1793 Go to original source... Go to PubMed...
  6. Gerasimov E.S., Kostygov A.Y., Yan S., Kolesnikov A.A. 2012: From cryptogene to gene? ND8 editing domain reduction in insect trypanosomatids. Eur. J. Protistol. 48: 185-193 Go to original source... Go to PubMed...
  7. Gluenz E., Shaw M.K., Gull K. 2007: Structural asymmetry and discrete nucleic acid subdomains in the Trypanosoma brucei kinetoplast. Mol. Microbiol. 64: 1529-1539 Go to original source... Go to PubMed...
  8. Guilbride L., Myler P.J., Stuart K. 1992: Distribution and sequence divergence of LRV1 viruses among different Leishmania species. Mol. Biochem. Parasitol. 54: 101-104 Go to original source... Go to PubMed...
  9. Guindon S., Delsuc F., Dufayard J.F., Gascuel O. 2009: Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol. 537: 113-137 Go to original source... Go to PubMed...
  10. 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 Go to original source... Go to PubMed...
  11. Harris K.A., Jr., Crothers D.M., Ullu E. 1995: In vivo structural analysis of spliced leader RNAs in Trypanosoma bruceiand Leptomonas collosoma: a flexible structure that is independent of cap4 methylations. RNA 1: 351-362 Go to PubMed...
  12. Hartley M.A., Ronet C., Zangger H., Beverley S.M., Fasel N. 2012: Leishmania RNA virus: when the host pays the toll. Front. Cell. Infect. Microbiol. 2: 99 Go to original source... Go to PubMed...
  13. Hollar L., Lukes J., Maslov D.A. 1998: Monophyly of endosymbiont containing trypanosomatids: phylogeny versus taxonomy. J. Eukaryot. Microbiol. 45: 293-297 Go to original source... Go to PubMed...
  14. Ilg T., Stierhof Y.D., Etges R., Adrian M., Harbecke D., Overath P. 1991: Secreted acid phosphatase of Leishmania mexicana: a filamentous phosphoglycoprotein polymer. Proc. Natl. Acad. Sci. USA 88: 8774-8778 Go to original source...
  15. Ives A., Ronet C., Prevel F., Ruzzante G., Fuertes-Marraco S., Schutz F., Zangger H., Revaz-Breton M., Lye L.F., Hickerson S.M., Beverley S.M., Acha-Orbea H., Launois P., Fasel N., Masina S. 2011: Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 331: 775-778 Go to original source... Go to PubMed...
  16. Jirku M., Yurchenko V.Y., Lukes J., Maslov D.A. 2012: New species of insect trypanosomatids from Costa Rica and the proposal for a new subfamily within the Trypanosomatidae. J. Eukaryot. Microbiol. 59: 537-547 Go to original source... Go to PubMed...
  17. Kostygov A.Y., Slisarenko E.P., Merkulov P.A., Podlipaev S.A. 2004: Genetic diversity of insect trypanosomatids from subarctic and North-West Russia revealed by UP-PCR typing. Protistology 3: 257-264
  18. Lukes J., Guilbride D.L., Votypka J., Zikova A., Benne R., Englund P.T. 2002: Kinetoplast DNA network: evolution of an improbable structure. Euk. Cell 1: 495-502 Go to original source...
  19. Malysheva M.N., Frolov A.O. 2004: [The description of Wallaceina vicina sp. n. (Kinetoplastida: Trypanosomatidae), from the water strider Gerris rufoscutellatus Latreille, 1807 (Hemiptera: Gerridae).] Parazitologiya 38: 470-476. (In Russian.)
  20. Malysheva M.N., Frolov A.O. 2009: [On the problem of identification of homoxenous trypanosome cultures with the description of a new species Wallaceina podlipaevi sp. n. (Kinetoplastida: Trypanosomatidae).] Parazitologiya 43: 502-515. (In Russian.)
  21. Mandelboim M., Estrano C.L., Tschudi C., Ullu E., Michaeli S. 2002: On the role of exon and intron sequences in trans-splicing utilization and cap 4 modification of the trypanosomatid Leptomonas collosoma SL RNA. J. Biol. Chem. 277: 35210-35218 Go to original source... Go to PubMed...
  22. Maslov D.A., Lukes J., Jirku M., Simpson L. 1996: Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Mol. Biochem. Parasitol. 75: 197-205 Go to original source... Go to PubMed...
  23. Maslov D.A., Podlipaev S.A., Lukes J. 2001: Phylogeny of the Kinetoplastida: taxonomic problems and insights into the evolution of parasitism. Mem. Inst. Oswaldo Cruz 96: 397-402 Go to original source... Go to PubMed...
  24. Maslov D.A., Votypka J., Yurchenko V., Lukes J. 2013: Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol. 29: 43-52 Go to original source... Go to PubMed...
  25. Maslov D.A., Westenberger S.J., Xu X., Campbell D.A., Sturm N.R. 2007: Discovery and barcoding by analysis of spliced leader RNA gene sequences of new isolates of Trypanosomatidae from Heteroptera in Costa Rica and Ecuador. J. Eukaryot. Microbiol. 54: 57-65 Go to original source... Go to PubMed...
  26. Maslov D.A., Yurchenko V.Y., Jirku M., Lukes J. 2010: Two new species of trypanosomatid parasites isolated from Heteroptera in Costa Rica. J. Eukaryot. Microbiol. 57: 177-188 Go to original source... Go to PubMed...
  27. 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 rRNA genes: polyphyly of Leptomonas and Blastocrithidia. J. Eukaryot. Microbiol. 48: 161-169 Go to original source... Go to PubMed...
  28. Morio F., Reynes J., Dollet M., Pratlong F., Dedet J.P., Ravel C. 2008: Isolation of a protozoan parasite genetically related to the insect trypanosomatid Herpetomonas samuelpessoai from a human immunodeficiency virus-positive patient. J. Clin. Microbiol. 46: 3845-3847 Go to original source... Go to PubMed...
  29. Moyne G. 1980: Methods in ultrastructural cytochemistry of the cell nucleus. Prog. Histochem. Cytochem. 13: 1-72 Go to original source... Go to PubMed...
  30. Obornik M., Vancova M., Lai D.H., Janouskovec J., Keeling P.J., Lukes J. 2011: Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of Apicomplexa, Chromera velia. Protist 162: 115-130 Go to original source... Go to PubMed...
  31. Podlipaev S.A. 1990: [Catalogue of World Fauna of Trypanosomatidae (Protozoa).] Zoologicheskii Institut AN SSSR, Leningrad, 178 pp. (In Russian.)
  32. Podlipaev S.A. 2001: The more insect trypanosomatids under study - the more diverse Trypanosomatidae appears. Int. J. Parasitol. 31: 648-652 Go to original source... Go to PubMed...
  33. Podlipaev S.A., Frolov A.O. 2000: [The phylogeny of the Trypanosomatidae: molecular and morphological approaches]. Parazitologiya 34: 169-182. (In Russian.)
  34. Podlipaev S.A., Frolov A.O., Kolesnikov A.A. 1990: [Proteomonas inconstans n. gen. n. sp. (Kinetoplastida, Trypanosomatidae), a parasite of the bug Calocoris sexguttatus (Hemiptera, Miridae).] Parazitologiya 24: 339-345. (In Russian.)
  35. Podlipaev S.A., Malysheva M.N., Kolesnikov A.A. 1991: Leptomonas rigidus sp. n. (Trypanosomatidae) - a parasite of Salda littoralis L. (Hemiptera, Heteroptera). Acta Protozool. 30: 121-127
  36. Podlipaev S.A., Sturm N.R., Fiala I., Fernandes O., Westenberger S.J., Dollet M., Campbell D.A., Lukes J. 2004: Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. J. Eukaryot. Microbiol. 51: 283-290 Go to original source... Go to PubMed...
  37. Posada D., Crandall K.A. 1998: MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818 Go to original source... Go to PubMed...
  38. Richter K. 1994: Cutting artefacts on ultrathin cryosections of biological bulk specimens. Micron 25: 297-308 Go to original source... Go to PubMed...
  39. Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. 2012: MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539-542 Go to original source... Go to PubMed...
  40. Salinas G., Zamora M., Stuart K., Saravia N. 1996: Leishmania RNA viruses in Leishmania of the Viannia subgenus. Am. J. Trop. Med. Hyg. 54: 425-429 Go to PubMed...
  41. Seligman A.M., Wasserkrug H.L., Hanker J.S. 1966: A new staining method (OTO) for enhancing contrast of lipid-containing membranes and droplets in osmium tetroxide-fixed tissue with osmiophilic thiocarbohydrazide (TCH). J. Cell Biol. 30: 424-432 Go to original source... Go to PubMed...
  42. Singh N., Chikara S., Sundar S. 2013: SOLiD sequencing of genomes of clinical isolates of Leishmania donovani from India confirm Leptomonas co-infection and raise some key questions. PLOS One 8: e55738 Go to original source... Go to PubMed...
  43. Srivastava P., Prajapati V.K., Vanaerschot M., Van der Auwera G., Dujardin J.C., Sundar S. 2010: Detection of Leptomonas sp. parasites in clinical isolates of Kala-azar patients from India. Infect. Genet. Evol. 10: 1145-1150 Go to original source... Go to PubMed...
  44. Stierhof Y.D., Ilg T., Russell D.G., Hohenberg H., Overath P. 1994: Characterization of polymer release from the flagellar pocket of Leishmania mexicana promastigotes. J. Cell Biol. 125: 321-331 Go to original source... Go to PubMed...
  45. Stinson S., Sommer J.R., Blum J.J. 1989: Morphology of Leishmania braziliensis: changes during reversible heat-induced transformation from promastigote to an ellipsoidal form. J. Parasitol. 75: 431-440 Go to original source... Go to PubMed...
  46. Svobodova M., Zidkova L., Cepicka I., Obornik M., Lukes J., Votypka J. 2007: Sergeia podlipaevi gen. nov., sp. nov. (Trypanosomatidae, Kinetoplastida), a parasite of biting midges (Ceratopogonidae, Diptera). Int. J. Syst. Evol. Microbiol. 57: 423-432 Go to original source... Go to PubMed...
  47. Swofford D.L. 2001: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4., Sinauer Associates, Sunderland, MA, USA
  48. Teixeira M.M., Borghesan T.C., Ferreira R.C., Santos M.A., Takata C.S., Campaner M., Nunes V.L., Milder R.V., de Souza W., Camargo E.P. 2011: Phylogenetic validation of the genera Angomonas and Strigomonas of trypanosomatids harboring bacterial endosymbionts with the description of new species of trypanosomatids and of proteobacterial symbionts. Protist 162: 503-524 Go to original source... Go to PubMed...
  49. Teixeira M.M., Takata C.S., Conchon I., Campaner M., Camargo E.P. 1997: Ribosomal and kDNA markers distinguish two subgroups of Herpetomonas among old species and new trypanosomatids isolated from flies. J. Parasitol. 83: 58-65 Go to original source... Go to PubMed...
  50. Thompson J.D., Gibson T.J., Higgins D.G. 2002: Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics Chapter 2: Unit 2 3 Go to PubMed...
  51. Tyc J., Votypka J., Klepetkova H., Sulakova H., Jirku M., Lukes J. 2013: Growing diversity of trypanosomatid parasites of flies (Diptera: Brachcera): frequent cosmopolitism and moderate host specificity. Mol. Phylogenet. Evol. 69: 255-264 Go to original source... Go to PubMed...
  52. Votypka J., Klepetkova H., Jirku M., Kment P., Lukes J. 2012a: Phylogenetic relationships of trypanosomatids parasitising true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int. J. Parasitol. 42: 489-500 Go to original source... Go to PubMed...
  53. Votypka J., Klepetkova H., Yurchenko V.Y., Horak A., Lukes J., Maslov D.A. 2012b: Cosmopolitan distribution of a trypanosomatid Leptomonas pyrrhocoris. Protist 163: 616-631 Go to original source... Go to PubMed...
  54. Votypka J., Maslov D.A., Yurchenko V., Jirku M., Kment P., Lun Z.R., Lukes J. 2010: Probing into the diversity of trypanosomatid flagellates parasitizing insect hosts in South-West China reveals both endemism and global dispersal. Mol. Phylogenet. Evol. 54: 243-253 Go to original source... Go to PubMed...
  55. Votypka J., Sukova E., Kraeva N., Ishemgulova A., Duzi I., Lukes J., Yurchenko V. 2013: Diversity of trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas gen. n. Protist 164: 763-781 Go to original source... Go to PubMed...
  56. Wallace F.G. 1966: The trypanosomatid parasites of insects and arachnids. Exp. Parasitol. 18: 124-193 Go to original source... Go to PubMed...
  57. Wallace F.G., Clark T.B., Dyer M.I., Collins T. 1960: Two new species of flagellates cultivated from insects of the genus Gerris. J. Protozool. 7: 390-392 Go to original source...
  58. Westenberger S.J., Sturm N.R., Yanega D., Podlipaev S.A., Zeledon 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 Go to original source... Go to PubMed...
  59. Willingham M.C., Rutherford A.V. 1984: The use of osmium-thiocarbohydrazide-osmium (OTO) and ferrocyanide-reduced osmium methods to enhance membrane contrast and preservation in cultured cells. J. Histochem. Cytochem. 32: 455-460 Go to original source... Go to PubMed...
  60. Yurchenko V.Y., Kolesnikov A.A. 2001: Minicircular kinetoplast DNA of Trypanosomatidae. Mol. Biol., Moscow 35: 3-13 Go to original source... Go to PubMed...
  61. Yurchenko V.Y., Lukes J., Jirku M., Maslov D.A. 2009: Selective recovery of the cultivation-prone components from mixed trypanosomatid infections: a case of several novel species isolated from Neotropical Heteroptera. Int. J. Syst. Evol. Microbiol. 59: 893-909 Go to original source... Go to PubMed...
  62. Yurchenko V.Y., Lukes J., Jirku M., Zeledon R., Maslov D.A. 2006a: Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania. Parasitology 133: 537-546 Go to original source... Go to PubMed...
  63. Yurchenko V.Y., Lukes J., Tesarova M., Jirku M., Maslov D.A. 2008: Morphological discordance of the new trypanosomatid species phylogenetically associated with the genus Crithidia. Protist 159: 99-114 Go to original source... Go to PubMed...
  64. Yurchenko V.Y., Lukes J., Xu X., Maslov D.A. 2006b: 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 Go to original source... Go to PubMed...
  65. Zamora M., Guilbride L., Sacks L., Stuart K. 2000: Phylogenetic analysis of the 5' subterminal region of isolates of Leishmania RNA virus-1. Ann. Trop. Med. Parasitol. 94: 123-133 Go to original source... Go to PubMed...
  66. Zamora M., Sacks L., Stuart K. 1995: Intracellular localization of LRV1 in infected Leishmania cells and epitope conservation of the coat protein. J. Eukaryot. Microbiol. 42: 580-582 Go to original source... Go to PubMed...
  67. Zangger H., Ronet C., Desponds C., Kuhlmann F.M., Robinson J., Hartley M.A., Prevel F., Castiglioni P., Pratlong F., Bastien P., Muller N., Parmentier L., Saravia N.G., Beverley S.M., Fasel N. 2013: Detection of Leishmania RNA virus in Leishmania parasites. PLoS Negl. Trop. Dis. 7: e2006 Go to original source... Go to PubMed...
  68. Zidkova L., Cepicka I., Votypka J., Svobodova M. 2010: Herpetomonas trimorpha sp. nov. (Trypanosomatidae, Kinetoplastida), a parasite of the biting midge Culicoides truncorum (Ceratopogonidae, Diptera). Int. J. Syst. Evol. Microbiol. 60: 2236-2246 Go to original source... Go to PubMed...