Abstract
Histomonas meleagridis is the etiological agent of histomonosis or blackhead disease. Recently, genotyping, based on polymerase chain reaction and sequencing of internal transcribed spacer-1 sequences was applied to various isolates originating from fowl. Three genotypes were described: types I and II isolates were associated with clinical disease and probably derived from H. meleagridis, whereas, type III isolates were not disease-associated and likely corresponded to Parahistomonas wenrichi according to morphological observations. However, this latter species has never been characterized at the molecular level and its phylogenetic relationships with other parabasalids remained hypothetical. To confirm the identification of these isolates, small subunit rRNA gene sequences were obtained from representatives of types I, II, and III and analyzed in a broad phylogeny including 64 other parabasalid sequences. From our phylogenetic trees, we confirmed that types I and II isolates were closely related, if not identical, to H. meleagridis, while type III isolates represented P. wenrichi. Both species clustered together with high support. This grouping suggested that speciation leading to these two species inhabiting the same hosts and ecological niche occurred recently in birds. In addition, speciation was likely followed by loss of pathogenicity in P. wenrichi.
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Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 120:399–451
Brugerolle G (1976) Cytologie ultrastructurale, systématique et évolution des Trichomonadida. Ann Station Biologique de Besse-en-Chandesse 10:1–90
Brugerolle G (1980) Etude ultrastructurale du flagellé Protrichomonas legeri (Léger 1905) parasite de l’estomac des Bogues (Box boops). Protistologica 17:431–438
Brugerolle G, Lee JJ (2001) Phylum Parabasalia. In: Lee JJ, Leedale GF, Patterson DJ, Bradbury PC (eds) The illustrated guide to the protozoa, 2nd edn. Allen Press, Lawrence, Kansas, pp 1196–1249
Carpenter KJ, Keeling PJ (2007) Morphology and phylogenetic position of Eucomonympha imla (Parabasalia: Hypermastigida). J Eukaryot Microbiol 54:325–332
Dufernez F, Walker RL, Noël C, Caby S, Mantini C, Delgado-Viscogliosi P, Ohkuma M, Kudo T, Capron M, Pierce RJ, Villanueva MR, Viscogliosi E (2007) Morphological and molecular identification of non-Tritrichomonas foetus trichomonad protozoa from the bovine preputial cavity. J Eukaryot Microbiol 54:161–168
Edgcomb VP, Viscogliosi E, Simpson AGB, Delgado-Viscogliosi P, Roger AJ, Sogin ML (1998) News insights into the phylogeny of trichomonads inferred from small subunit rRNA sequences. Protist 149:359–366
Gerbod D, Edgcomb VP, Noël C, Zenner L, Wintjens L, Delgado-Viscogliosi P, Holder ME, Sogin ML, Viscogliosi E (2001) Phylogenetic position of the trichomonad parasite of turkeys, Histomonas meleagridis (Smith) Tyzzer, inferred from small subunit rRNA sequence. J Eukaryot Microbiol 48:498–504
Gerbod D, Noël C, Dolan MF, Edgcomb VP, Kitade O, Noda S, Dufernez F, Ohkuma M, Kudo T, Capron M, Sogin ML, Viscogliosi E (2002) Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Devescovinidae and Calonymphidae (Trichomonadea). Mol Phylogenet Evol 25:545–556
Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559
Hampl V, Cepicka I, Flegr J, Tachezy J, Kulda J (2004) Critical analysis of the topology and rooting of the parabasalian 16 S rRNA tree. Mol Phylogenet Evol 32:711–723
Hampl V, Vrlik M, Cepicka I, Pecka Z, Kulda J, Tachezy J (2006) Affiliation of Cochlosoma to trichomonads confirmed by phylogenetic analysis of the small-subunit rRNA gene and a new family concept of the order Trichomonadida. Int J Syst Evol Microbiol 56:305–312
Hampl V, Cepicka I, Flegr J, Tachezy J, Kulda J (2007) Morphological and molecular diversity of the monocercomonadid genera Monocercomonas, Hexamastix, and Honigbergiella gen. nov. Protist 158:365–383
Honigberg BM (1963) Evolutionary and systematic relationships in the flagellate order Trichomonadida Kirby. J Protozool 10:20–63
Honigberg BM, Brugerolle G (1990) Structure. In: Honigberg BM (ed) Trichomonads parasitic in humans. Springer-Verlag, New-York, pp 5–35
Honigberg BM, Kuldova J (1969) Structure of a nonpathogenic histomonad from the cecum of galliform birds and revision of the trichomonad family Monocercomonadidae Kirby. J Protozool 16:526–535
Honigberg BM, Mattern CFT, Daniel WA (1971) Fine structure of the mastigont system in Tritrichomonas foetus (Riedmüller). J Protozool 18:183–198
Huelsenbeck JP, Ronquist F (2001) MrBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Keeling PJ (2002) Molecular phylogenetic position of Trichomitopsis termopsidis (Parabasalia) and evidence for the Trichomitopsiinae. Europ J Protistol 38:279–286
Lund EE (1963) Histomonas wenrichi n. sp. (Mastigophora: Mastigamoebidae), a non-pathogenic parasite of gallinaceous birds. J Protozool 10:401–404
Lund EE (1969) Histomoniasis. Adv Vet Sci Comp Med 13:355–390
Lund EE, Augustine PC, Chute AM (1967) Histomonas meleagridis after one thousand in vitro passages. J Protozool 14:349–351
Mattern CFT, Honigberg BM, Daniel WA (1967) The mastigont system of Trichomonas gallinae (Rivolta) as revealed by electron microscopy. J Protozool 14:320–339
McDougald LR (2003) Other protozoan diseases of the intestinal tract-histomoniasis (Blackhead). In: Saif YM, Barnes HJ, Glisson JR, Fadly AM, McDougald LR, Swayne DE (eds) Diseases of poultry, 11th edn. Iowa State University Press, Ames, pp 1001–1008
Noda S, Mantini C, Bordereau C, Kitade O, Dolan MF, Viscogliosi E, Ohkuma M (2009) Molecular phylogeny of parabasalids with emphasis on the order Cristamonadida and its complex morphological evolution. Mol Phylogenet Evol 52(1):217–224
Noël C, Noda S, Mantini C, Dolan MF, Moriya S, Delgado-Viscogliosi P, Kudo T, Capron M, Pierce RJ, Ohkuma M, Viscogliosi E (2007) Molecular phylogenetic position of the genera Stephanonympha and Caduceia (Parabasalia) inferred from nuclear small subunit rRNA gene sequences. J Eukaryot Microbiol 54:93–99
Ohkuma M, Iida T, Ohtoko K, Yuzawa H, Noda S, Viscogliosi E, Kudo T (2005) Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Hypermastigea. Mol Phylogenet Evol 35:646–655
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Reid WM (1967) Etiology and dissemination of the blackhead disease syndrome in turkeys and chickens. Exp Parasitol 21:249–275
Rybicka K, Honigberg BM, Holt SC (1972) Fine structure of the mastigont system in culture forms of Histomonas meleagridis (Smith). Protistologica 8:107–120
Saleudin ASM (1971) Fine structure of Tetratrichomonas limacis (Dujardin). Can J Zool 50:695–701
Schuster FL (1968) Ultrastructure of Histomonas meleagridis (Smith) Tyzzer, a parasitic amebo-flagellate. J Parasitol 54:725–737
Smith T (1895) An infectious disease among turkeys caused by protozoa (infectious entero-hepatitis). Bur Anim Ind USDA Bul 8:7–90
Tyzzer EE (1920) The flagellate character and reclassification of the parasite producing “blackhead” in turkeys–Histomonas (gen. nov.) meleagridis (Smith). J Parasitol 6:124–131
Tyzzer EE (1934) Studies on histomoniasis, or “blackhead” infection, in the chicken and the turkey. Proc Am Acad Arts Sci 69:189–264
Van der Heijden HMJF, McDougald LR, Landman WJM (2005) High field of parasites and prolonged in vitro culture of Histomonas meleagridis. Avian Pathol 34:505–508
Van der Heijden HMJF, Landman WJM, Greve S, Peek R (2006) Genotyping of Histomonas meleagridis isolates based on internal transcribed spacer-1 sequences. Avian Pathol 35:330–334
Wenrich DH (1943) Observations on the morphology of Histomonas (Protozoa, Mastigophora) from pheasants and chickens. J Morphol 72:279–304
Acknowledgements
This work was supported by the Institut Pasteur de Lille, the Institut National de la Santé et de la Recherche Médicale, the Centre National de la Recherche Scientifique, and the Université Lille Nord de France to E. V., Research Groups of Clean Chemistry and Bioarchitect in RIKEN to M. O., Grants-in-Aid for Scientific Research from Japan Society for the Promotion of Science to M. O. and S. N., and by a grant from the French Ministère de l’Education Nationale, de la Recherche et de la Technologie to C. M.
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Mantini, C., Dalia-Cornette, J., Noda, S. et al. Molecular identification and phylogenetic relationships of trichomonad isolates of galliform birds inferred from nuclear small subunit rRNA gene sequences. Parasitol Res 106, 163–170 (2009). https://doi.org/10.1007/s00436-009-1643-2
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DOI: https://doi.org/10.1007/s00436-009-1643-2