Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-22T06:21:29.723Z Has data issue: false hasContentIssue false
  • English
  • Français

First report of Trypanosoma dionisii (Trypanosomatidae) identified in Australia

Published online by Cambridge University Press:  28 September 2020

Jill M. Austen Open the ORCID record for Jill M. Austen [Opens in a new window] ,
Esther Van Kampen ,
Siobhon L. Egan ,
Mark A. O'Dea ,
Bethany Jackson ,
Una M. Ryan ,
Peter J. Irwin  and
Diana Prada
Jill M. Austen*
Affiliation:
Vector and Waterborne Pathogens Research Group, College of Science, Health, Engineering and Education, Murdoch University, Perth6150, Australia
Esther Van Kampen
Affiliation:
School of Veterinary Medicine, Murdoch University, Perth, WA6150, Australia
Siobhon L. Egan
Affiliation:
Vector and Waterborne Pathogens Research Group, College of Science, Health, Engineering and Education, Murdoch University, Perth6150, Australia
Mark A. O'Dea
Affiliation:
School of Veterinary Medicine, Murdoch University, Perth, WA6150, Australia
Bethany Jackson
Affiliation:
School of Veterinary Medicine, Murdoch University, Perth, WA6150, Australia
Una M. Ryan
Affiliation:
Vector and Waterborne Pathogens Research Group, College of Science, Health, Engineering and Education, Murdoch University, Perth6150, Australia
Peter J. Irwin
Affiliation:
Vector and Waterborne Pathogens Research Group, College of Science, Health, Engineering and Education, Murdoch University, Perth6150, Australia
Diana Prada
Affiliation:
School of Veterinary Medicine, Murdoch University, Perth, WA6150, Australia
*
Author for correspondence: Jill M. Austen, E-mail: J.Austen@murdoch.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Trypanosomes are blood-borne parasites that can infect a variety of different vertebrates, including animals and humans. This study aims to broaden scientific knowledge about the presence and biodiversity of trypanosomes in Australian bats. Molecular and morphological analysis was performed on 86 blood samples collected from seven different species of microbats in Western Australia. Phylogenetic analysis on 18S rDNA and glycosomal glyceraldehyde phosphate dehydrogenase (gGAPDH) sequences identified Trypanosoma dionisii in five different Australian native species of microbats; Chalinolobus gouldii, Chalinolobus morio, Nyctophilus geoffroyi, Nyctophilus major and Scotorepens balstoni. In addition, two novels, genetically distinct T. dionisii genotypes were detected and named T. dionisii genotype Aus 1 and T. dionisii genotype Aus 2. Genotype Aus 2 was the most prevalent and infected 20.9% (18/86) of bats in the present study, while genotype Aus 1 was less prevalent and was identified in 5.8% (5/86) of Australian bats. Morphological analysis was conducted on trypomastigotes identified in blood films, with morphological parameters consistent with trypanosome species in the subgenus Schizotrypanum. This is the first report of T. dionisii in Australia and in Australian native bats, which further contributes to the global distribution of this cosmopolitan bat trypanosome.

Keywords

AustraliaChalinolobus gouldiiChalinolobus moriomicrobatsNyctophilus geoffroyiNyctophilus majorScotorepens balstoniTrypanosoma dionisii
Type
Research Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1801 - 1809
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Austen, JM, Jefferies, R, Friend, JA, Ryan, U, Adams, P and Reid, SA (2009) Morphological and molecular characterization of Trypanosoma Copemani N. sp (Trypanosomatidae) isolated from Gilbert's potoroo (Potorous gilbertii) and quokka (Setonix Brachyurus). Parasitology 136, 783–792.CrossRefGoogle Scholar
Austen, JM, O'Dea, M, Jackson, B and Ryan, U (2015) High prevalence of Trypanosoma vegrandis in bats from Western Australia. Veterinary Parasitology 214, 342–7.CrossRefGoogle ScholarPubMed
Backhouse, TC and Bolliger, A (1951) Transmission of Chagas' disease to the Australian marsupial Trichosurus Vulpecula. Transactions of the Royal Society of Tropical Medicine and Hygiene 44, 521–33.10.1016/0035-9203(51)90032-6CrossRefGoogle ScholarPubMed
Baker, JR, Green, SM, Chaloner, LA and Gaborak, M (1972) Trypanosoma (Schizotrypanum) dionisii of Pipistrellus Pipistrellus (chiroptera): intra-and extracellular development in vitro. Parasitology 65, 251–63.CrossRefGoogle ScholarPubMed
Barbosa, AD, Mackie, JT, Stenner, R, Gillett, A, Irwin, P and Ryan, U (2016) Trypanosoma teixeirae: a new species belonging to the T. cruzi Clade causing trypanosomosis in an Australian little red flying fox (Pteropus Scapulatus). Veterinary Parasitology 223, 214–21.CrossRefGoogle Scholar
Beltz, LA (2017) Kinetoplastids and Bats. Bats and Human Health: Ebola, SARS, Rabies and Beyond. New York, NY, USA: John Wiley & Sons.CrossRefGoogle Scholar
Benson, DA, Cavanaugh, M, Clark, K, Karsch-Mizrachi, I, Lipman, DJ, Ostell, J and Sayers, EW (2017) Genbank. Nucleic Acids Research 45, D37–D42.CrossRefGoogle ScholarPubMed
Breinl, A (1913) Parasite protozoa encountered in the blood of Australian native animals. The Australian Institute of Tropical Medicine 1191, 30–38.Google Scholar
Castresana, J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology Evolution 17, 540–52.CrossRefGoogle ScholarPubMed
Cavazzana, M Jr, Marcili, A, Lima, L, da Silva, FM, Junqueira, ACV, Veludo, HH, Viola, LB, Campaner, M, Nunes, VLB, Paiva, F, Coura, JR, Camargo, EP and 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. International Journal for Parasitology 40, 345–55.CrossRefGoogle ScholarPubMed
Churchill, S (2008) Australian Bats, 2nd Edn. Crows Nest, N.S.W.: Allen & Unwin.Google Scholar
Constantine, DG (2003) Geographic translocation of bats: known and potential problems. Emerging Infectious Diseases 9, 17–21.CrossRefGoogle ScholarPubMed
Dario, MA, Rodrigues, MS, Barros, JH, Xavier, SC, D'Andrea, PS, Roque, AL and Jansen, AM (2016) Ecological scenario and Trypanosoma cruzi DTU characterization of a fatal acute Chagas disease case transmitted orally (Espirito Santo state, Brazil). Parasite and Vectors 9, 477.CrossRefGoogle Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–7.CrossRefGoogle ScholarPubMed
Egan, SL, Taylor, CL, Austen, JM, Banks, PB, Ahlstrom, LA, Ryan, UM, Irwin, PJ and Oskam, CL (2020) Molecular identification of the Trypanosoma (Herpetosoma) lewisi Clade in black rats (Rattus Rattus) from Australia. Parasitology Research 119, 1691–1696.CrossRefGoogle ScholarPubMed
Espinosa-Alvarez, O, Ortiz, PA, Lima, L, Costa-Martins, AG, Serrano, MG, Herder, S, Buck, GA, Camargo, EP, Hamilton, PB, Stevens, JR and Teixeira, MMG (2018) Trypanosoma Rangeli is phylogenetically closer to Old World trypanosomes than to Trypanosoma cruzi. International Journal for Parasitology 48, 569–584.CrossRefGoogle ScholarPubMed
Garcia, L, Ortiz, S, Osorio, G, Torrico, MC, Torrico, F and Solari, A (2012) Phylogenetic analysis of Bolivian bat trypanosomes of the subgenus Schizotrypanum based on cytochrome b Sequence and minicircle analyses. PLoS One 7, e36578.CrossRefGoogle ScholarPubMed
Gardner, RA and Molyneux, DH (1988) Trypanosoma (Megatrypanum) incertum From Pipistrellus Pipistrellus: development and transmission by cimicid bugs. Parasitology 96, 433–47.CrossRefGoogle ScholarPubMed
Hamilton, PB, Stevens, JR, Gaunt, MW, Gidley, J and Gibson, WC (2004) Trypanosomes are monophyletic; evidence from genes to glyceraldehde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 1393–1404.CrossRefGoogle ScholarPubMed
Hamilton, PB, Stevens, JR, Gidley, J, Holz, P and Gibson, WC (2005) A new lineage of trypanosomes from Australian vertebrates and terrestrial bloodsucking leeches (Haemadipsidae). International Journal for Parasitology 35, 431–443.CrossRefGoogle Scholar
Hamilton, PB, Gibson, WC and Stevens, JR (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Molecular Phylogenetics and Evolution 44, 15–25.CrossRefGoogle ScholarPubMed
Hamilton, PB, Cruickshank, C, Stevens, JR, Teixeira, MMG and Mathews, F (2012a) Parasites reveal movement of bats between the New and Old Worlds. Molecular Phylogenetics and Evolution 63, 521–6.CrossRefGoogle Scholar
Hamilton, PB, Teixeira, MMG and Stevens, JR (2012b) The evolution of Trypanosoma Cruzi: the ‘bat seeding’ hypothesis. Trends in Parasitology 28, 136–41.CrossRefGoogle Scholar
Hoare, C (1972) The Trypanosomes of Mammals. A Zoological Monograph. Oxford, England: Blackwell Scientific Publishing.Google Scholar
Hodo, CL, Goodwin, CC, Mayes, BC, Mariscal, JA, Waldrup, KA and Hamer, SA (2016) Trypanosome species, including Trypanosoma Cruzi, in sylvatic and peridomestic bats of Texas, USA. Acta Tropica 164, 259–266.CrossRefGoogle ScholarPubMed
Hornok, S, Kovacs, R, Meli, ML, Gonczi, E, Hofmann-Lehmann, R, Kontschan, J, Gyuranecz, M, Dan, A and Molnar, V (2012) First detection of bartonellae in a broad range of bat ectoparasites. Veterinary Microbiology 159, 541–3.CrossRefGoogle Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–9.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–4.10.1093/molbev/msw054CrossRefGoogle ScholarPubMed
Lima, L, Silva, FM, Neves, L, Attias, M, Takata, CS, Campaner, M, de Souza, W, Hamilton, PB and 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, 856–72.CrossRefGoogle ScholarPubMed
Lima, L, Espinosa-Alvarez, O, Hamilton, PB, Neves, L, Takata, CS, Campaner, M, Attias, M, de Souza, W, Camargo, EP and Teixeira, MMG (2013) Trypanosoma livingstonei: a new species from African bats supports the bat seeding hypothesis for the Trypanosoma Cruzi clade. Parasites and Vectors 6, 221.CrossRefGoogle ScholarPubMed
Lukes, J, Jirku, M, Dolezel, D, Kralova, I, Hollar, L and Maslov, DA (1997) Analysis of ribosomal RNA genes suggests that trypanosomes are monophyletic. Journal of Molecular Evolution 44, 521–527.CrossRefGoogle ScholarPubMed
Mackerras, MJ (1959) The haematozoa of Australian mammals. Australian Journal of Zoology 7, 105–135.CrossRefGoogle Scholar
Mackie, JT, Stenner, R, Gillett, AK, Barbosa, A, Ryan, U and Irwin, PJ (2017) Trypanosomiasis in an Australian little red flying fox (Pteropus Scapulatus). Australian Veterinary Journal 95, 259–261.CrossRefGoogle Scholar
Macphee, RD and Greenwood, AD (2013) Infectious disease, endangerment, and extinction. International Journal of Evolutionary Biology 2013, 571939, 1–9. doi: https://doi.org/10.1155/2013/571939CrossRefGoogle ScholarPubMed
Maeda, FY, Cortez, C, Alves, RM and Yoshida, N (2012) Mammalian cell invasion by closely related Trypanosoma species T. dionisii And T. cruzi. Acta Tropica 121, 141–7.CrossRefGoogle Scholar
Mafie, E, Rupa, FH, Takano, A, Suzuki, K, Maeda, K and Sato, H (2018) First record of Trypanosoma Dionisii of the T. cruzi Clade from the Eastern bent-winged bat (Miniopterus fuliginosus) in the Far East. Parasitology Research 117, 673–680.CrossRefGoogle Scholar
Maslov, DA, Lukes, J, Jirku, M and 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. Molecular and Biochemical Parasitology 75, 197–205.CrossRefGoogle ScholarPubMed
Mcinnes, LM, Gillett, A, Ryan, UM, Austen, J, Campbell, RSF, Hanger, J and Reid, SA (2009) Trypanosoma Irwini N. sp (Sarcomastigophora: Trypanosomatidae) from the koala (Phascolarctos cinereus). Parasitology 136, 875–885.CrossRefGoogle Scholar
Molyneux, DH (1969) The fine-structure of the epimastigote forms of Trypanosoma Lewisi in the rectum of the flea, Nosopsyllus fasciatus. Parasitology 59, 55–66.CrossRefGoogle ScholarPubMed
Morgulis, A, Coulouris, G, Raytselis, Y, Madden, TL, Agarwala, R and Schäffer, AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics (Oxford, England) 24, 1757–1764.CrossRefGoogle ScholarPubMed
Myers, N, Mittermeier, RA, Mittermeier, CG, da Fonseca, GA and Kent, J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853–8.CrossRefGoogle ScholarPubMed
Nei, M and Kumar, S (2000) Molecular Evolution and Phylogenetics. New York: Oxford University Press.Google Scholar
Noyes, HA, Stevens, JR, Teixeira, M, Phelan, J and Holz, P (1999) A nested PCR for the ssrRNA gene detects Trypanosoma Binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331–339.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Hohna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–42.CrossRefGoogle ScholarPubMed
Rozsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal for Parasitology 86, 228–232.CrossRefGoogle ScholarPubMed
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH image to Image J: 25 years of image analysis. Nature Methods 9, 671–675.CrossRefGoogle Scholar
Stevens, J, Noyes, H and Gibson, W (1998) The evolution of trypanosomes infecting humans and primates. Memorias do Instituto Oswaldo Cruz 93, 669–676.CrossRefGoogle ScholarPubMed
Stevens, JR, Noyes, H, Dover, GA and Gibson, WC (1999) The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.CrossRefGoogle ScholarPubMed
Szentiványi, T, Christe, P and Glaizot, O (2019) Bat flies and their microparasites:current knowledge and distribution. Frontiers in Veterinary Science 6. doi:10.3389/fvets.2019.00115.CrossRefGoogle ScholarPubMed
Tamura, K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Molecular Biology and Evolution 9, 678–87.Google ScholarPubMed
Teeling, EC, Springer, MS, Madsen, O, Bates, P, O'brien, SJ and Murphy, WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science (New York, N.Y.) 307, 580–4.CrossRefGoogle ScholarPubMed
Thekisoe, OM, Honda, T, Fujita, H, Battsetseg, B, Hatta, T, Fujisaki, K, Sugimoto, C and Inoue, N (2007) A trypanosome species isolated from naturally infected Haemaphysalis Hystricis Ticks in Kagoshima Prefecture, Japan. Parasitology 134, 967–974.CrossRefGoogle ScholarPubMed
Tyler, KM and Engman, DM (2001) The life cycle of Trypanosoma Cruzi Revisited. International Journal for Parasitology 31, 472–81.CrossRefGoogle ScholarPubMed
Wang, LJ, Han, HJ, Zhao, M, Liu, JW, Luo, LM, Wen, HL, Qin, XR, Zhou, CM, Qi, R, Yu, H and Yu, XJ (2019) Trypanosoma Dionisii in insectivorous bats from northern China. Acta Tropica 193, 124–128.CrossRefGoogle ScholarPubMed
Wyatt, KB, Campos, PF, Gilbert, MT, Kolokotronis, SO, Hynes, WH, Desalle, R, Ball, SJ, Daszak, P, Macphee, RD and Greenwood, AD (2008) Historical mammal extinction on Christmas Island (Indian ocean) correlates with introduced infectious disease. PLoS One 3, e3602.CrossRefGoogle ScholarPubMed
Yang, R, Murphy, C, Song, Y, Ng-Hublin, J, Estcourt, A, Hijjawi, N, Chalmers, R, Hadfield, S, Bath, A, Gordon, C and Ryan, U (2013) Specific and quantitative detection and identification of Cryptosporidium hominis and C. parvum in clinical and environmental samples. Experimental Parasitology 135, 142–7.CrossRefGoogle Scholar
Zhang, Z, Schwartz, S, Wagner, L and Miller, W (2000) A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7, 203–214.CrossRefGoogle ScholarPubMed
Supplementary material: File

Austen et al. supplementary material

Austen et al. supplementary material 1

Download Austen et al. supplementary material(File)
File 19 KB
Supplementary material: File

Austen et al. supplementary material

Austen et al. supplementary material 2

Download Austen et al. supplementary material(File)
File 2.8 MB