Parasitology Research

, Volume 117, Issue 3, pp 673–680 | Cite as

First record of Trypanosoma dionisii of the T. cruzi clade from the Eastern bent-winged bat (Miniopterus fuliginosus) in the Far East

  • Eliakunda Mafie
  • Fatema Hashem Rupa
  • Ai Takano
  • Kazuo Suzuki
  • Ken Maeda
  • Hiroshi SatoEmail author
Original Paper


Chiropteran mammals worldwide harbour trypanosomes (Euglenozoa: Kinetoplastea: Trypanosomatida) of the subgenus ‘Schizotrypanum’ in the classical sense. Latterly, these trypanosomes have been referred to as members of the ‘Trypanosoma cruzi clade’ as their phylogenetic relationships, structure and life cycle conform to T. cruzi, parasitising various terrestrial mammals as well as humans in Latin America. Little is known, however, about the trypanosome species in Asian bats. During a survey on Borrelia spp. in the Eastern bent-winged bat (Miniopterus fuliginosus) living in a cave in Wakayama Prefecture, Japan, incidental proliferation of trypanosomes was detected in two of 94 haemocultures. Squat or slender trypanosomes that proliferated in the cultures were 7.5–20.5 μm in length between both body ends and 1.0–3.8 μm in width with/without free flagella up to 14.5 μm (n = 29). The nucleotide sequences of the small subunit ribosomal RNA gene (SSU rDNA; 2176 bp), large subunit ribosomal RNA gene (1365 bp) and glycosomal glyceraldehyde-3-phosphate dehydrogenase gene (gGAPDH; 843 bp) of the present isolates were characterized to clarify their molecular phylogenetic position in T. cruzi-like trypanosomes. The newly obtained SSU rDNA and gGAPDH nucleotide sequences showed the highest identities with Brazilian and European isolates of Trypanosoma dionisii of the T. cruzi clade, ranging between 99.4 and 99.7% or between 95.6 and 99.3% identities, respectively. Although multiple T. dionisii isolates from the North and South American continents showed the closest molecular genetic relatedness to the present Far East isolates, only short SSU rDNA segments of the former isolates were deposited. Therefore, a definitive conclusion cannot be made until full nucleotide sequencing of at least the American isolates’ SSU rDNA is available. This is the first confirmation of a Far East distribution of T. dionisii, demonstrating a wide geographical distribution of the species in the Eurasian and American continents with a limited nucleotide variation.


Trypanosoma dionisii Schizotrypanum T. cruzi clade Miniopterus fuliginosus Japan rDNA gGAPDH Molecular genetic variation 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55(4):539–552. CrossRefPubMedGoogle Scholar
  2. Baker JR, Chaloner LA, Green SM (1971) Intracellular development in vitro of Trypanosoma dionisii of bats. Trans R Soc Trop Med Hyg 65:427Google Scholar
  3. Baker JR, Green SM, Chaloner LA, Gaborak M (1972) Trypanosoma (Schizotrypanum) dionisii of Pipistrellus pipistrellus (Chiroptera): intra- and extracellular development in vitro. Parasitology 65(2):251–263.
  4. Bern C, Kjos S, Yabsley MJ, Montgomery SP (2011) Trypanosoma cruzi and Chagas’ disease in the United States. Clin Microbiol Rev 24(4):655–681. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Botero A, Cooper C, Thompson CK, Clode PL, Rose K, Thompson RCA (2016) Morphological and phylogenetic description of Trypanosoma noyesi sp. nov.: an Australian wildlife trypanosome within the T. cruzi clade. Protist 167(5):425–439. CrossRefPubMedGoogle Scholar
  6. Cavazzana M Jr, Marcili A, Lima L, Maia da Silva F, Junqueira ÂCV, Veludo HH, Viola LB, Campaner M, Nunes VLB, Paiva F, Coura JR, Camargo EP, Teixeira MMG (2010) 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 40(3):345–355. CrossRefPubMedGoogle Scholar
  7. Dario MA, Rodrigues MS, Barros JH, Xavier SC, D’Andrea PS, Roque AL, Jansen AM (2016) Ecological scenario and Trypanosoma cruzi DTU characterization of a fatal acute Chagas disease case transmitted orally (Espírito Santo state, Brazil). Parasit Vectors 9(1):477. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O (2008) robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469CrossRefGoogle Scholar
  9. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704. CrossRefPubMedGoogle Scholar
  10. Hamilton PB, Stevens JR, Gaunt MW, Gidley J, Gibson WC (2004) Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. Int J Parasitol 34(12):1393–1404. CrossRefPubMedGoogle Scholar
  11. Hamilton PB, Gibson WC, Stevens JR (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Mol Phylogenet Evol 43:15–25Google Scholar
  12. Hamilton PB, Teixeira MMG, Stevens JR (2012a) The evolution of Trypanosoma cruzi: the ‘bat seeding’ hypothesis. Trends Parasitol 28(4):136–141. CrossRefPubMedGoogle Scholar
  13. Hamilton PB, Cruickshank C, Stevens JR, Teixeira MMG, Mathews F (2012b) Parasites reveal movement of bats between the New and Old Worlds. Mol Phylogenet Evol 63(2):521–526. CrossRefPubMedGoogle Scholar
  14. Hoare CA (1972) The trypanosomes of mammals: a zoological monograph. Blackwell Scientific Publications, Oxford, U.K., 749 pGoogle Scholar
  15. Hodo CL, Goodwin CC, Mayes BC, Mariscal JA, Waldrup KA, Hamer SA (2016) Trypanosome species, including Trypanosoma cruzi, in sylvatic and peridomestic bats or Texas, USA. Acta Trop 164:259–266. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kirchhoff LV (2011) Epidemiology of American trypanosomiasis (Chagas disease). Adv Parasitol 75:1–18. CrossRefPubMedGoogle Scholar
  17. Lima L, Maia da Silva F, Neves L, Attias M, Takata CSZ, Campaner M, de Souza W, Hamilton PB, Teixeira MMG (2012) Evolutionary insights from bat trypanosomes: morphological, developmental and phylogenetic evidence of a new species, Trypanosoma (Schizotrypanum) erneyi sp. nov., in African bats closely related to Trypanosoma (Schizotrypanum) cruzi and allied species Protist 163: 856–872, 6, DOI:
  18. Lima L, Espinosa-Álvarez O, Hamilton PB, Neves L, Takata CSA, Campaner M, Attias, M, de Souza W, Camargo EP, Teixeira MMG (2013) Trypanosoma livingstonei: a new species from African bats supports the bat seeding hypothesis for the Trypanosoma cruzi clade. Parasit Vectors 6:221 [https://www.parasitesand]
  19. Lima L, Espinosa-Álvarez O, Pinto M, Cavazzana M Jr, Pavan AC, Carranza JC, Lim BK, Campaner M, Takata CSA, Camargo EP, Hamilton PB, Teixeira MMG (2015) New insights into the evolution of the Trypanosoma cruzi clade provided by a new trypanosome species tightly linked to Neotropical Pteronotus bats and related to an Australian lineage of trypanosomes. Parasit Vectors 8(1):657. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Maia da Silva F, Marcilli A, Lima L, Cvazzana M Jr, Ortiz PA, Campaner M, Takeda GF, Paiva F, Nunes VLB, Camargo EP, Teizeira MMG (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 Trop 109(3):199–207. CrossRefPubMedGoogle Scholar
  21. Marcili A, da Costa AP, Soares HS, Acosta ICL, Lima JTR, Minervino AHH, Melo ATL, Agular DM, Pacheco RC, Gennari SM (2013) Isolation and phylogenetic relationships of bat trypanosomes from different biomes in Mato Grosso, Brazil. J Parasitol 99(6):1071–1076. CrossRefPubMedGoogle Scholar
  22. Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T (2010) The wild mammals of Japan. Shoukadoh book Sellers, Kyoto, Japan, p 544Google Scholar
  23. Oliveira MPC, Cortex M, Maeda FY, Fernandes MC, Haapalainen EF, Yoshida N (2009) Unique behavior of Trypanosoma dionisii interacting with mammalian cells: invasion, intracellular growth, and nuclear localization. Acta Trop 110(1):65–74. CrossRefPubMedGoogle Scholar
  24. Sato H, Osanai A, Kamiya H, Obara Y, Jiang W, Zhen Q, Chai J, Une Y, Ito M (2005) Characterization of SSU and LSU rRNA genes of three Trypanosoma (Herpetosoma) grosi isolates maintained in Mongolian jirds. Parastiology 130(2):157–167. CrossRefGoogle Scholar
  25. Sato H, Leo N, Katakai Y, Takano J, Akari H, Nakamura S, Une Y (2008) Prevalence and molecular phylogenetic characterization of Trypanosoma (Megatrypanum) minasense in the peripheral blood of small Neotropical primates after a quarantine period. J Parasitol 94(5):1128–1138. CrossRefPubMedGoogle Scholar
  26. Sato H, Takano A, Kawabata H, Une Y, Watanabe H, Mukhtar M (2009) Trypanosoma cf. varani in an imported ball python (Python reginus) from Ghana. J Parasitol 95(4):1029–1033. CrossRefPubMedGoogle Scholar
  27. Stevens J, Noyes H, Gibson W (1998) The evolution of trypanosomes infecting humans and primates. Mem Inst Oswald Cruz 93(5):669–676. CrossRefGoogle Scholar
  28. Takano A, Nakao M, Masuzawa T, Takada N, Yano Y, Ishiguro F, Fujita H, Ito T, Ma X, Oikawa Y, Kawamori F, Kumagai K, Mikami T, Hanaoka N, Ando S, Honda N, Taylor K, Tsubota T, Konnai S, Watanabe H, Ohnishi M, Kawabata H (2011) Multilocus sequence typing implicates rodents as the main reservoir host of human-pathogenic Borrelia garinii in Japan. J Clin Microbiol 49(5):2035–2039. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ziccardi M, Lourenço-de-Oliveira R, Nogueira R (1996) The haemoculture of Trypanosoma minasense Chagas, 1908. Mem Inst Oswaldo Cruz 91(4):501–505. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Eliakunda Mafie
    • 1
  • Fatema Hashem Rupa
    • 1
  • Ai Takano
    • 2
  • Kazuo Suzuki
    • 3
  • Ken Maeda
    • 2
  • Hiroshi Sato
    • 1
    Email author
  1. 1.Laboratory of Parasitology, United Graduate School of Veterinary ScienceYamaguchi UniversityYamaguchiJapan
  2. 2.Laboratory of Microbiology, Joint Faculty of Veterinary MedicineYamaguchi UniversityYamaguchiJapan
  3. 3.Hikiiwa Park CentreTanabeJapan

Personalised recommendations