Mem Inst Oswaldo Cruz, Rio de Janeiro, VOLUME 115 | MAY 2020
Original Article

Analysing ambiguities in trypanosomatids taxonomy by barcoding

Carolina Boucinha1, Amanda R Caetano1, Helena LC Santos1, Raphael Helaers2, Miikka Vikkula2, Marta Helena Branquinha3, André Luis Souza dos Santos3, Philippe Grellier4, Karina Alessandra Morelli1,5, +, Claudia Masini d‘Avila-Levy1,2, +

1Fundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Laboratório de Estudos Integrados em Protozoologia,
Coleção de Protozoários da Fiocruz, Rio de Janeiro, RJ, Brasil
2University of Louvain, de Duve Institute, Laboratory of Human Molecular Genetics, Brussels, Belgium
3Universidade Federal do Rio de Janeiro, Instituto de Microbiologia Paulo de Góes, Rio de Janeiro, Brasil
4Muséum National d‘Histoire Naturelle, Unité Molécules de Communication et Adaptation des Microorganisme, Paris, France
5Universidade do Estado do Rio de Janeiro, Instituto de Biologia Roberto Alcântara Gomes, Departamento de Ecologia, Rio de Janeiro, RJ, Brasil

DOI: 10.1590/0074-02760200504

BACKGROUND Biodiversity screens and phylogenetic studies are dependent on reliable DNA sequences in public databases. Biological collections possess vouchered specimens with a traceable history. Therefore, DNA sequencing of samples available at institutional collections can greatly contribute to taxonomy, and studies on evolution and biodiversity.
METHODS We sequenced part of the glycosomal glyceraldehyde phosphate dehydrogenase (gGAPDH) and the SSU rRNA (V7/V8) genes from 102 trypanosomatid cultures, which are available on request at
OBJECTIVE The main objective of this work was to use phylogenetic inferences, using the obtained DNA sequences and those from representatives of all Trypanosomatidae genera, to generate phylogenetic trees that can simplify new isolates screenings.
FINDINGS A DNA sequence is provided for the first time for several isolates, the phylogenetic analysis allowed the classification or reclassification of several specimens, identification of candidates for new genera and species, as well as the taxonomic validation of several deposits.
MAIN CONCLUSIONS This survey aimed at presenting a list of validated species and their associated DNA sequences combined with a short historical overview of each isolate, which can support taxonomic and biodiversity research and promote culture collections.

01. Wallace FG. The trypanosomatid parasites of insects and arachnids. Exp Parasitol. 1966; 18(1): 124-93.
02. Vickerman K. The evolutionary expansion of the trypanosomatid flagellates. Int J Parasitol. 1994; 24(8): 1317-31.
03. d’Avila-Levy CM, Boucinha C, Kostygov A, Santos HL, Morelli KA, Grybchuk-Ieremenko A, et al. Exploring the environmental diversity of kinetoplastid flagellates in the high-throughput DNA sequencing era. Mem Inst Oswaldo Cruz. 2015; 110(8): 956-65.
04. Hamilton PT, Votýpka J, Dostalova A, Yurchenko V, Bird NH, Lukeš J, et al. Infection dynamics and immune response in a newly described drosophila-trypanosomatid association. MBio. 2015; 6(5): e01356-15.
05. Yurchenko V, Kostygov A, Havlova J, Grybchuk-Ieremenko A, Sevcikova T, Lukeš J, et al. Diversity of trypanosomatids in cockroaches and the description of Herpetomonas tarakana sp. n. J Eukaryot Microbiol. 2016; 63(2): 198-209.
06. Espinosa OA, Serrano MG, Camargo EP, Teixeira MMG, Shaw JJ. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2018; 145(4): 430-42.
07. Kostygov AY, Dobakova E, Grybchuk-Ieremenko A, Vahala D, Maslov DA, Votýpka J, et al. Novel trypanosomatid-bacterium association: evolution of endosymbiosis in action. MBio. 2016; 7(2): e01985.
08. Kostygov AY, Yurchenko V. Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol (Praha). 2017; 64: 2017.020.
09. Camargo EP. Phytomonas and other trypanosomatid parasites of plants and fruit. Adv Parasitol. 1999; 42: 29-112.
10. Zanetti A, Ferreira RC, Serrano MG, Takata CS, Campaner M, Attias M, et al. Phytomonas (Euglenozoa: Trypanosomatidae): phylogenetic analyses support infrageneric lineages and a new species transmitted to Solanaceae fruits by a pentatomid hemipteran. Eur J Protistol. 2016; 56: 232-49.
11. Podlipaev S. Catalogue of world fauna of Trypanosomatidae (Protozoa) (in Russian). Proc Zool Inst Leningrad. 1990; 217: 1-178.
12. Teixeira MM, Borghesan TC, Ferreira RC, Santos MA, Takata CS, Campaner M, et al. 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. 2011; 162(3): 503-24.
13. Borghesan TC, Ferreira RC, Takata CS, Campaner M, Borda CC, Paiva F, et al. Molecular phylogenetic redefinition of Herpetomonas (Kinetoplastea, Trypanosomatidae), a genus of insect parasites associated with flies. Protist. 2013; 164(1): 129-52.
14. Votýpka J, d’Avila-Levy CM, Grellier P, Maslov DA, Lukeš J, Yurchenko V. New approaches to systematics of trypanosomatidae: criteria for taxonomic (re)description. Trends Parasitol. 2015; 31(10): 460-9.
15. d’Avila-Levy CM, Yurchenko V, Votýpka J, Grellier P. Protist collections: essential for future research. Trends Parasitol. 2016; 32(11): 840-2.
16. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005; 33(2): 511-8.
17. Helaers R, Milinkovitch MC. MetaPIGA v2.0: maximum likelihood large phylogeny estimation using the metapopulation genetic algorithm and other stochastic heuristics. BMC Bioinformatics. 2010; 11: 379.
18. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012; 61(3): 539-42.
19. Carvalho AL, Deane MP. Trypanosomatidae isolated from Zelus leucogrammus (Perty, 1834) (Hemiptera, Reduviidae), with a discussion on flagellates of insectivorous bugs. J Protozool. 1974; 21(1): 5-8.
20. Faria e Silva PM, Sole-Cava AM, Soares MJ, Motta MC, Fiorini JE, de Souza W. Herpetomonas roitmani (Fiorini et al., 1989) n. comb.: a trypanosomatid with a bacterium-like endosymbiont in the cytoplasm. J Protozool. 1991; 38(5): 489-94.
21. Fiorini JE, Silva PMF, Soares MJ, Brazil RP. [Three new species of trypanosomatidae isolated in Alfenas, Minas Gerais, Brazil]. Mem Inst Oswaldo Cruz. 1989; 84(1): 69-74.
22. Fiorini JE, Takata CS, Teofilo VM, Nascimento LC, Faria-e-Silva PM, Soares MJ, et al. Morphological, biochemical and molecular characterization of Herpetomonas samuelpessoai camargoi n. sub sp., a trypanosomatid isolated from the flower of the squash Cucurbita moschata. J Eukaryot Microbiol. 2001; 48(1): 62‐9.
23. Yurchenko VY, Lukeš J, Tesarova M, Jirků M, Maslov DA. Morphological discordance of the new trypanosomatid species phylogenetically associated with the genus Crithidia. Protist. 2008; 159(1): 99-114.
24. Schmid-Hempel R, Tognazzo M. Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. J Eukaryot Microbiol. 2010; 57(4): 337-45.
25. Kostygov AY, Grybchuk-Ieremenko A, Malysheva MN, Frolov AO, Yurchenko V. Molecular revision of the genus Wallaceina. Protist. 2014; 165(5): 594-604.
26. Wallace FG, Clark TB, Dyer MI, Collins T. Two new species of flagellates cultivated from insects of the genus Gerris. J Protozool. 1960; 7(4): 390-2.
27. Andersen NM. Phylogeny and taxonomy of water striders, genus Aquarius Schellenberg (Insecta, Hemiptera, Gerridae), with a new species from Australia. Steenstrupia. 1990; 16(4): 37-81.
28. Hanson WL, McGhee RB. The biology and morphology of Crithidia acanthocephali n. sp., Leptomonas zeptoglossi n. sp., and Blastocrithidia euschisti n. sp. J Protozool. 1961; 8(2): 200-4.
29. Langridge DF, McGhee RB. Crithidia mellificae n. sp. an acidophilic trypanosomatid of the honey bee Apis mellifera. J Protozool. 1967; 14(3): 485-7.
30. Runckel C, DeRisi J, Flenniken ML. A draft genome of the honey bee trypanosomatid parasite Crithidia mellificae. PLoS One. 2014; 9(4): e95057.
31. Cepero A, Ravoet J, Gómez-Moracho T, Bernal JL, Del Nozal MJ, Bartolomé C, et al. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Res Notes. 2014; 7(1): 649.
32. Schwarz RS, Bauchan GR, Murphy CA, Ravoet J, de Graaf DC, Evans JD. Characterization of two species of trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, and Lotmaria passim n. gen., n. sp. J Eukaryot Microbiol. 2015; 62(5): 567-83.
33. Lipa JJ, Triggiani O. Crithidia bombi sp n, a new flagellated parasite of a bumble bee Bombus terrestris L (Hymenoptera, Apidae). Acta Protozool. 1988; 27: 287-90.
34. Léger L. Sur un flagellé parasite de l’Anopheles maculipennis. C RSéances Soc Biol Fil. 1902; 54: 354-6.
35. Wallace FG. Flagellate parasites of mosquitoes with special reference to Crithidia fasciculata Leger, 1902. J Parasitol. 1943; 29(3): 196-205.
36. Noguchi H, Tilden EB. Comparative studies of herpetomonads and leishmanias: I. Cultivation of herpetomonads from insects and plants. J Exp Med. 1926; 44(3): 307-25.
37. Simpson AM, Simpson L. Isolation and characterization of kinetoplast DNA networks and minicircles from Crithidia fasciculata. J Protozool. 1974; 21(5): 774-81.
38. Hannaert V, Opperdoes FR, Michels PA. Comparison and evolutionary analysis of the glycosomal glyceraldehyde-3-phosphate dehydrogenase from different Kinetoplastida. J Mol Evol. 1998; 47(6): 728-38.
39. Soares MJ, Brazil RP, Tanuri A, Souza W. Some ultrastructural aspects of Crithidia guilhermei n. sp. isolated from Phaenicia cuprina (Diptera: Calliphoridae). Can J Zool. 1986; 64(12): 2837-42.
40. Sibajev A, Pacheco RS, Soares MJ, Cupolillo E, dos Santos AB, Momen H. Crithidia ricardoi sp. n. a new species of trypanosomatidae isolated from Culex saltanensis Dyar, 1928 (Diptera: Culicidae). Mem Inst Oswaldo Cruz. 1993; 88(4): 541-5.
41. Maruyama SR, de Santana AKM, Takamiya NT, Takahashi TY, Rogerio LA, Oliveira CAB, et al. Non-leishmania parasite in fatal visceral leishmaniasis-like disease, Brazil. Emerg Infect Dis. 2019; 25(11): 2088-92.
42. Roitman I, Mundim MH, Azevedo HP, Kitajima EW. Growth of Crithidia at high temperature: Crithidia hutneri sp. n. and Crithidia luciliae thermophila s. sp. n. J Protozool. 1977; 24(4): 553-6.
43. Ishemgulova A, Butenko A, Kortisova L, Boucinha C, Grybchuk- Ieremenko A, Morelli KA, et al. Molecular mechanisms of thermal resistance of the insect trypanosomatid Crithidia thermophila. PLoS One. 2017; 12(3): e0174165.
44. Sá-Xavier C, Santos SM, Sousa MA. A new trypanosomatid belonging to the genus Crithidia isolated from Zelus leucogrammus (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz. 1998; 93(Suppl. II): 95
45. Teixeira MM, Takata CS, Conchon I, Campaner M, Camargo EP. Ribosomal and kDNA markers distinguish two subgroups of Herpetomonas among old species and new trypanosomatids isolated from flies. J Parasitol. 1997; 83(1): 58-65.
46. Wallace FG, Todd SR, Rogers W. Flagellate parasites of water striders with a description of Leptomonas costoris, n. sp. J Protozool. 1965; 12(3): 390-3.
47. Roubaud E. Sur un nouveau flagellé parasite de líntestin des muscides au Congo français. C RSéances Soc Biol Fil. 1908; 64: 1106-8.
48. Wallace FG, Todd SR. Leptomonas Mirabilis Roubaud 1908 in a Central American Blowfly. J Protozool. 1964; 11(5): 502-5.
49. Wenyon CM. Protozoology. A manual for medical men, veterinarians and zoologists. Vol. I. London: Bailliére, Tindall & Cox; 1926.
50. Pereira SMS. Elaboração de protocolos para padronização e sistematização dos procedimentos para recebimento de depósitos de novas amostras na coleção de protozoários da FIOCRUZ. Rio de Janeiro: Universidade Federal do Rio de Janeiro; 2019. 270 pp.
51. Rogers WE, Wallace FG. Two new subspecies of Herpetomonas muscarum (Leidy, 1856) Kent, 1880. J Protozool. 1971; 18(4): 645-9.
52. Podlipaev SA. Insect trypanosomatids: the need to know more. Mem Inst Oswaldo Cruz. 2000; 95(4): 517-22.
53. Seixas RLR, Ponte CS, Santos GPL, Brazil RP. Isolation of Leishmania sp. of Nectomys squamipes (Rodentia: Cricetidae) from Catimbau Grande, municipality of Rio Bonito, Rio de Janeiro State. In: XXI Annual Meeting on Basic Research of Chaga’s Disease, 1994. Caxambu: 1994. p. 79.
54. Attias M, de Souza W. Axenic cultivation and ultrastructural study of a Phytomonas sp. isolated from the milkweed plant Euphorbia hyssopifolia. J Protozool. 1986; 33(1): 84-7.
55. Galvão AB, Oliveira RL, Carvalho ALM, Veiga GP. Leptomonas pessoai sp. n. (Trypanosomatidae, Kinetoplastida, Protozoa). Rev Goiana Med. 1970; 16: 229-36.
56. Manaia AC, Souza MCM, Lustosa ES, Roitman I. Leptomonas lactosovorans n. sp., a lactose-utilizing trypanosomatid: description and nutritional requirements. J Protozool. 1981; 28(1): 124-6.
57. Romeiro A, Sole-Cava A, Sousa MA, de Souza W, Attias M. Ultrastructural and biochemical characterization of promastigote and cystic forms of Leptomonas wallacei n. sp. isolated from the intestine of its natural host Oncopeltus fasciatus (Hemiptera: Lygaeidae). J Eukaryot Microbiol. 2000; 47(3): 208-20.
58. Suwannayod S, Sanit S, Sukontason K, Sukontason KL. Parasarcophaga (Liopygia) ruficornis (Diptera:Sarcophagidae): a flesh fly species of medical importance. Trop Biomed. 2013; 30(2): 174-80.
59. Votýpka J, Kostygov AY, Kraeva N, Grybchuk-Ieremenko A, Tesařová M, Grybchuk D, et al. Kentomonas gen. n., a new genus of endosymbiont-containing trypanosomatids of strigomonadinae subfam. n. Protist. 2014; 165(6): 825-38.
60. Yoshida N, Freymüller E, Wallace FG. Herpetomonas mariadeanei sp. n. (Protozoa, Trypanosomatidae) from Muscina stabulans Fallen, 1816 (Diptera, Muscidae). J Protozool. 1978; 25(4): 421-5.
61. Jirků M, Yurchenko VY, Lukeš J, Maslov DA. New species of insect trypanosomatids from Costa Rica and the proposal for a new subfamily within the trypanosomatidae. J Eukaryot Microbiol. 2012; 59(6): 537-47.
62. Yurchenko VY, Lukeš J, Jirků M, Maslov DA. 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. 2009; 59(Pt 4): 893-909.
63. Manaia AC, Cordeiro NS. Description and axenic cultivation of an insect trypanosomatid. Annals of XVI Annual Meeting on Basic Research of Chaga’s Disease, 1989; 84(Suppl. II): 151.
64. Votýpka J, Klepetkova H, Jirků M, Kment P, Lukeš J. Phylogenetic relationships of trypanosomatids parasitising true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int J Parasitol. 2012; 42(5): 489-500.
65. Wallace FG. Leptomonas seymouri sp. n. from the cotton stainer Dysdercus suturellus. JProtozool. 1977; 24(4): 483-4.
66. Aragão H. Sur un flagellé du latex de Manihot palmata, Phytomonas francai n. sp. C RSéances Soc Biol Ses Fil. 1927; 97: 1077-80.
67. Vainstein MH, Roitman I. Cultivation of Phytomonas françai associated with poor development of root system of cassava. J Protozool. 1986; 33(4): 511-3.
68. Dollet M, Cambrony D, Gargani D. Culture axénique in vitro de Phytomonas sp. (Trypanosomatidae) d’Euphorbe, transmis par Stenocephalus agilis Scop (Coreide). C R Acad Sci III. 1982; 295: 547-50.
69. Gibbs AJ. Leptomonas serpens n. sp., parasitic in the digestive tract and salivary glands of Nezara viridula (Pentatomidae) and in the sap of Solanum lycopersicum (tomato) and other plants. Parasitology. 1957; 47(3-4): 297-303.
70. Podlipaev SA. Phytomonas elmassiani (Mastigophora: Trypanosomamonadida) from the plant Cynanchum sibiricum (Asclepiadaceae) in Central Asia and Kazakhstan (in Russian). Proc Zool Inst Acad Sci USSR. 1986; 144: 61-5.
71. Brazil RP, Fiorini JE, Faria-e-Silva P. Phytomonas sp. a trypanosomatid parasite of tomato, isolated from salivary glands of Phthia picta (Hemiptera: Coreidae) in southeast Brazil. Mem Inst Oswaldo Cruz. 1990; 85(2): 239-40.
72. Jankevicius JV, Jankevicius SI, Campaner M, Conchon I, Maeda LA, Teixeira MMG, et al. Life cycle and culturing of Phytomonas serpens (Gibbs), a trypanosomatid parasite of tomatoes. J Protozool. 1989; 36(3): 265-71.
73. Sá-Carvalho D, Perez-Morga D, Traub-Cseko YM. Characterization of kinetoplast DNA from Phytomonas serpens. J Eukaryot Microbiol. 1993; 40(3): 317-22.
74. Conchon I, Campaner M, Sbravat C, Camargo EP. Trypanosomatids, other than Phytomonas spp., isolated and cultured from fruit. J Protozool. 1989; 36(4): 412-4.
75. Burstein ZA, Romero OR. Flagelados en el latex de la Jatropha macrantha (Huanarpo Hembra). Arch Per Pat Clin. 1956; 10: 1-12.
76. Jankevicius SI, De Almeida IL, Jankevicius JV, Cavazzana JrM, Attias M, De Souza W. Axenic cultivation of trypanosomatids found in corn (Zea mays) and in phytophagous hemipterans (Leptoglossus zonatus Coreidae) and their experimental transmission. J Euk Microbiol. 1993; 40(5): 576-81.
77. Novy FG, MacNeal WJ, Torrey HN. The trypanosomes of mosquitoes and other insects. J Infect Dis. 1907; 4(2): 223-76.
78. Wallace FG, Johnson A. The infectivity of old cultured strains of mosquito flagellates. J-Insect Pathol. 1961; 3: 75-80.
79. Chang KP. Ultrastructure of symbiotic bacteria in normal and antibiotic-treated Blastocrithidia culicis and Crithidia oncopelti. J Protozool. 1974; 21(5): 699-707.
80. Frolov A, Malysheva M. Description of Crithidia allae sp. n. and Crithidia brevicula sp. n. (Protozoa, Trypanosomatidae) from the predator bug Nabis brevis Scholtz (Hemiplera, Miridae) (in Russian). Russ J Zool. 1989; 68: 5-10.
81. Yurchenko V, Votýpka J, Tesarova M, Klepetkova H, Kraeva N, Jirků M, et al. Ultrastructure and molecular phylogeny of four new species of monoxenous trypanosomatids from flies (Diptera: Brachycera) with redefinition of the genus Wallaceina. Folia Parasitol (Praha). 2014; 61(2): 97-112.
82. Yurchenko VY, Lukeš J, Jirků M, Zeledon R, Maslov DA. Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania. Parasitology. 2006; 133(Pt 5): 537-46.
83. Barratt J, Kaufer A, Peters B, Craig D, Lawrence A, Roberts T, et al. Isolation of novel trypanosomatid, Zelonia australiensis sp. nov. (Kinetoplastida: Trypanosomatidae) provides support for a Gondwanan origin of dixenous parasitism in the Leishmaniinae. PLoS Negl Trop Dis. 2017; 11(1): e0005215.
84. Dedet JP, Geoffroy B, Benichou JC. Herpetomonas dedonderi N. Sp. (Sarcomastigophora, Trypanosomatidae) from Haemagogus janthinomys Dyar, 1921 (Diptera, Culicidae). J Protozool. 1986; 33(4): 530-3.
85. Svobodova M, Zidkova L, Cepicka I, Obornik M, Lukeš J, Votýpka J. Sergeia podlipaevi gen. nov., sp. nov. (Trypanosomatidae, Kinetoplastida), a parasite of biting midges (Ceratopogonidae, Diptera). Int J Syst Evol Microbiol. 2007; 57(Pt 2): 423-32
86. Votýpka J, Sukova E, Kraeva N, Ishemgulova A, Duzi I, Lukeš J, et al. Diversity of trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas gen. n. Protist. 2013; 164(6): 763-81.
87. Kostygov A, Frolov AO. [Leptomonas jaculum (Leger, 1902) Woodcock 1914: a leptomonas or a blastocrithidia?] (in Russian). Parazitologiia. 2007; 41(2): 126-36.
88. Fiorini JE, Cucolichio G, Rezende D, Alves SR, Faria e Silva PM, Soares MJ, et al. Morphological characterization of a Phytomonas sp. isolated from a Cucurbita flower. In: XXII Annual Meeting on Basic Research of Chaga’s Disease, 1995. Caxambu: 1994. p. 258.
89. Wallace FG, Clark TB. Flagellate parasites of the fly, Phaenicia sericata. J Protozool. 1959; 6(1): 58-61.
90. Dagget PM, Dollahon N, Janovy J. Herpetomonas megaseliae sp. n. (Protozoa: Trypanosomatidae) from Megaselia scalaris (Loew, 1866) Schmitz, 1929 (Diptera: Phoridae). J Parasitol. 1972; 58(5): 946-9.
91. Mcghee RB, Postell F. Axenic cultivation of Phytomonas davidi Lafont (Trypanosomatidae). A symbiote of lacticiferous plants (Euphorbiaceae). J Protozool. 1976; 23(2): 238-40.
92. Fiorini JE, Faria e Silva PM, Brazil RP, Roitman I, Angluster J, De Souza W, et al. Detection of trypanosomatids in the Solanum gilo and Solanum lycopersicum in Alfenas, MG, Brazil. In: XIV Annual Meeting on Basic Research of Chaga’s Disease, 1986. Caxambu. p. 33.
93. Roitman I, Brener Z, Roitman C, Kitajima EW. Demonstration that Leptomonas pessoai. Galvão, Oliveira, Carvalho & Veiga, 1970, is a Herpetomonas. J Protozool. 1976; 23(2): 291-3.
94. Zotta G. Sur un flagellé du type Herpetomonas chez Pyrrhocoris apterus. Ann Sci Univ Jassy. 1912; 7: 211-23.
95. Kraeva N, Butenko A, Hlaváčová J, Kostygov A, Myškova J, Grybchuk D, et al. Leptomonas seymouri: adaptations to the dixenous life cycle analyzed by genome sequencing, transcriptome profiling and co-infection with Leishmania donovani. PLoS Path. 2015: 11(8): e1005127.
96. Frolov A, Malysheva M, Yurchenko V, Kostygov A. Back to monoxeny: Phytomonas nordicus descended from dixenous plant parasites. Eur J Protistol. 2016; 52(1): 1-10.
97. Kastelein P, Camargo EP. Trypanosomatid protozoa in fruit of solanaceae in southeastern Brazil. Mem Inst Oswaldo Cruz. 1990; 85(4): 413-7.
98. Maslov DA, Yurchenko VY, Jirků M, Lukeš J. Two new species of trypanosomatid parasites isolated from Heteroptera in Costa Rica. J Eukaryot Microbiol. 2010; 57(2): 177-88.
99. Beard CB, Butler JF, Greiner EC. In vitro growth, characterization and host-parasite relationship of Leptomonas pulexsimulantis n. sp., a trypanosomatid flagellate of the flea Pulex simulans. J Parasitol. 1989; 75(5): 658-68.
100. Carvalho ALM. Estudos sobre a posição sistemática, a biologia e a transmissão de tripanosomatídeos encontrados em Zelus leucogrammus (Perty, 1834) (Hemiptera, Reduviidae). Rev Patol Trop. 1973; 2(2): 223-74.
101. Marcili A, Speranca MA, Da Costa AP, Madeira MF, Soares HS, Sanches CO, et al. Phylogenetic relationships of Leishmania species based on trypanosomatid barcode (SSU rDNA) and gGAPDH genes: taxonomic revision of Leishmania (L.) infantum chagasi in South America. Infect Genet Evol. 2014; 25: 44-51.
102. Muniz J, Medina HSG. Leishmaniose tegumentar do cobaio (Leishmania enriettii n.sp.). Arq Biol Tecnol. 1948: 3(2): 13-35.
103. Lainson R, Shaw JJ. Evolution, classification and geographical distribution. In: Peters W, Killick-Kendrick R, editors. The leishmaniases in biology and medicine. London: Academic Press Inc; 1987. 1-120.
104. Flegontov P, Votýpka J, Skalický T, Logacheva MD, Penin AA, Tanifuji G, et al. Paratrypanosoma is a novel early-branching Trypanosomatid. Current Biology. 2013; 23(18): 1787-93.
105. Dollet M, Sturm NR, Campbell DA. The spliced leader RNA gene array in phloem-restricted plant trypanosomatids (Phytomonas) partitions into two Trypanosomatid biodiversity in Costa Rica 9 major groupings: epidemiological implications. Parasitology. 2001; 122(Pt3): 289-97.
106. Sanchez-Moreno M, Fernandez-Becerra C, Mascaro C, Rosales MJ, Dollet M, Osuna A. Isolation, in vitro culture, ultrastructure study, and characterization by lectin-agglutination tests of Phytomonas isolated from tomatoes (Lycopersicon esculentum) and cherimoyas (Anona cherimolia) in southeastern Spain. Parasitol Res. 1995; 81(7): 575-81.
107. Hollar L, Lukeš J, Maslov DA. Monophyly of endosymbiont containing trypanosomatids: phylogeny versus taxonomy. J Eukaryot Microbiol. 1998; 45(3): 293-97.
108. Cavazzana Jr M, Marcili A, Lima L, da Silva FM, Junqueira AC, Veludo HH, et al. Phylogeographical, ecological and biological patterns shown by nuclear (ssrRNA and gGAPDH) and mitochondrial (Cyt b) genes of trypanosomes of the subgenus Schizotrypanum parasitic in Brazilian bats. Int J Parasitol. 2010; 40(3): 345-55.
109. Chagas C. Nova trypanozomiaze humana. Estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Mem Inst Oswaldo Cruz. 1909; 1(2): 159-218.

Financial support: CNPq, CAPES, FAPERJ.
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Received 23 January 2020
Accepted 06 May 2020

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sala 201, Manguinhos, 21040-900 
Rio de Janeiro, RJ, Brazil

Tel.: +55-21-2562-1222

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