Sequence analyses at mitochondrial and nuclear loci reveal a novel Theileria sp. and aid in the phylogenetic resolution of piroplasms from Australian marsupials and ticks


Autoři: Amanda D. Barbosa aff001;  Jill Austen aff001;  Timothy J. Portas aff003;  J. Anthony Friend aff004;  Liisa A. Ahlstrom aff005;  Charlotte L. Oskam aff001;  Una M. Ryan aff001;  Peter J. Irwin aff001
Působiště autorů: Vector- and Water-Borne Pathogen Research Group, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, WA, Australia aff001;  CAPES Foundation, Ministry of Education of Brazil, Brasília—DF, Brazil aff002;  Veterinary and Research Centre, Tidbinbilla Nature Reserve, Australian Capital Territory, Australia aff003;  Department of Biodiversity, Conservation and Attractions, Albany, WA, Australia aff004;  Bayer Australia Ltd, Pymble, Australia aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225822

Souhrn

The order Piroplasmida encompasses two main families: Babesiidae and Theileriidae, containing tick-borne pathogens of veterinary and medical importance worldwide. While only three genera (Babesia, Cytauxzoon and Theileria) comprising piroplasm parasites are currently recognised, phylogenetic studies at the 18S rRNA (18S) gene suggest that these organisms represent at least ten lineages, one of which comprises the relatively unique and highly diverse Theileria spp. from Australian marsupials and ticks. As an alternative to analysing 18S sequences alone, sequencing of mitochondrial genes has proven to be useful for the elucidation of evolutionary relationships amongst some groups of piroplasms. This research aimed to characterise piroplasms from Australian native mammals and ticks using multiple genetic markers (18S, cytochrome c, oxidase subunit III (cox3) and cytochrome B (cytB)) and microscopy. For this, nearly complete piroplasm-18S sequences were obtained from 32 animals belonging to six marsupial species: eastern bettong (Bettongia gaimardi), eastern quoll (Dasyurus viverrinus), eastern grey kangaroo (Macropus giganteus), swamp wallaby (Wallabia bicolor), quokka (Setonix brachyurus) and Gilbert’s potoroo (Potorous gilbertii). The organisms detected represented eight novel Theileria genotypes, which formed five sub-clades within the main marsupial clade containing previously reported Australian marsupial and tick-derived Theileria spp. A selection of both novel and previously described Australian piroplasms at the 18S were also successfully characterised, for the first time, at the cox3 and cytB loci, and corroborated the position of Australian native theilerias in a separate, well-supported clade. Analyses of the cox3 and cytB genes also aided in the taxonomic resolution within the clade of Australian Piroplasmida. Importantly, microscopy and molecular analysis at multiple loci led to the discovery of a unique piroplasm species that clustered with the Australian marsupial theilerias, for which we propose the name Theileria lupei n. sp.

Klíčová slova:

Babesia – DNA sequence analysis – Genetic loci – Phylogenetic analysis – Sequence alignment – Sequence analysis – Theileria – Marsupials


Zdroje

1. Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA. Babesia: a world emerging. Infect Genet Evol. 2012;12(8):1788–809. doi: 10.1016/j.meegid.2012.07.004 22871652

2. Solano-Gallego L, Baneth G. Babesiosis in dogs and cats-expanding parasitological and clinical spectra. Vet Parasitol. 2011;181(1):48–60. doi: 10.1016/j.vetpar.2011.04.023 21571435

3. Lee JY, Ryan UM, Jefferies R, McInnes LM, Forshaw D, Friend JA, et al. Theileria gilberti n. sp. (Apicomplexa: Theileriidae) in the Gilbert's potoroo (Potorous gilbertii). J Eukaryot Microbiol 2009;56(3):290–5. doi: 10.1111/j.1550-7408.2009.00398.x 19527357

4. Rong J, Bunce M, Wayne A, Pacioni C, Ryan U, Irwin P. A high prevalence of Theileria penicillata in woylies (Bettongia penicillata). Exp Parasitol. 2012;131(2):157–61. doi: 10.1016/j.exppara.2012.03.013 22465500

5. Barbosa A, Irwin P, Ryan U. Haemoprotozoan parasites. In: Volgenest L, Portas T, editors. Current therapy in Medicine of Australian Mammals. Sydney: CSIRO; 2019. p. 43–56.

6. Loh SM, Egan S, Gillett A, Banks PB, Ryan UM, Irwin PJ, et al. Molecular surveillance of piroplasms in ticks from small and medium-sized urban and peri-urban mammals in Australia. Int J Parasitol Parasites Wildl. 2018;7(2):197–203. doi: 10.1016/j.ijppaw.2018.05.005 29988853

7. Greay TL, Zahedi A, Krige AS, Owens JM, Rees RL, Ryan UM, et al. Endemic, exotic and novel apicomplexan parasites detected during a national study of ticks from companion animals in Australia. Parasit Vectors. 2018;11(1):197. doi: 10.1186/s13071-018-2775-y 29558984

8. Schreeg ME, Marr HS, Tarigo JL, Cohn LA, Bird DM, Scholl EH, et al. Mitochondrial Genome Sequences and Structures Aid in the Resolution of Piroplasmida phylogeny. PLoS One. 2016;11(11):e0165702. doi: 10.1371/journal.pone.0165702 27832128

9. O'Donoghue P. Haemoprotozoa: Making biological sense of molecular phylogenies. Int J Parasitol Parasites Wildl. 2017;6(3):241–56. doi: 10.1016/j.ijppaw.2017.08.007 28913164

10. Neitz WO, Thomas AD. Cytauxzoon sylvicaprae gen. nov., spec. nov., a protozoon responsible for a hitherto undescribed disease in the duiker, Sylvicapra grimmia (Linne). Onderstepoort J Vet Sci Anim Ind. 1948;23(1–2):63–76. 18863433

11. Reichard MV, Van Den Bussche RA, Meinkoth JH, Hoover JP, Kocan AA. A new species of Cytauxzoon from Pallas' cats caught in Mongolia and comments on the systematics and taxonomy of piroplasmids. J Parasitol. 2005;91(2):420–6. doi: 10.1645/GE-384R 15986619

12. Chauvin A, Moreau E, Bonnet S, Plantard O, Malandrin L. Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission. Vet Res. 2009;40(2):37. doi: 10.1051/vetres/2009020 19379662

13. Homer MJ, Aguilar-Delfin I, Telford SR III, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev. 2000;13:451–69. doi: 10.1128/cmr.13.3.451-469.2000 10885987

14. Harris DJ. New species need characters: comments on recently described apicomplexan parasites from Australia. Parasit Vectors. 2019;12(1):172. doi: 10.1186/s13071-019-3424-9 30992062

15. Jalovecka M, Sojka D, Ascencio M, Schnittger L. Babesia Life Cycle—When Phylogeny Meets Biology. Trends Parasitol. 2019.

16. Allsopp MT, Allsopp BA. Molecular sequence evidence for the reclassification of some Babesia species. Ann N Y Acad Sci. 2006;1081:509–17. doi: 10.1196/annals.1373.076 17135560

17. Criado-Fornelio A, Martinez-Marcos A, Buling-Sarana A, Barba-Carretero JC. Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part II. Phylogenetic analysis and evolutionary history. Vet Parasitol. 2003;114(3):173–94. doi: 10.1016/s0304-4017(03)00141-9 12788253

18. Lack JB, Reichard MV, Van Den Bussche RA. Phylogeny and evolution of the Piroplasmida as inferred from 18S rRNA sequences. Int J Parasitol. 2012;42(4):353–63. doi: 10.1016/j.ijpara.2012.02.005 22429769

19. Paparini A, Macgregor J, Ryan UM, Irwin PJ. First Molecular Characterization of Theileria ornithorhynchi Mackerras, 1959: yet Another Challenge to the Systematics of the Piroplasms. Protist. 2015;166(6):609–20. doi: 10.1016/j.protis.2015.10.001 26599724

20. Paparini A, Ryan UM, Warren K, McInnes LM, de Tores P, Irwin PJ. Identification of novel Babesia and Theileria genotypes in the endangered marsupials, the woylie (Bettongia penicillata ogilbyi) and boodie (Bettongia lesueur). Exp Parasitol. 2012;131(1):25–30. doi: 10.1016/j.exppara.2012.02.021 22433913

21. Šlapeta J, Saverimuttu S, Vogelnest L, Sangster C, Hulst F, Rose K, et al. Deep-sequencing to resolve complex diversity of apicomplexan parasites in platypuses and echidnas: Proof of principle for wildlife disease investigation. Infect Genet Evol. 2017;55:218–27. doi: 10.1016/j.meegid.2017.09.007 28919547

22. Dayrat B. Towards integrative taxonomy. Biol J Linn Soc. 2005;85:407–15.

23. Austen JM, Reid SA, Robinson DR, Friend JA, Ditcham WG, Irwin PJ, et al. Investigation of the morphological diversity of the potentially zoonotic Trypanosoma copemani in quokkas and Gilbert's potoroos. Parasitology. 2015;142(11):1443–52. doi: 10.1017/S0031182015000785 26160545

24. Jefferies R, Ryan UM, Irwin PJ. PCR-RFLP for the detection and differentiation of the canine piroplasm species and its use with filter paper-based technologies. Vet Parasitol. 2007;144(1–2):20–7. doi: 10.1016/j.vetpar.2006.09.022 17127005

25. Yang R, Murphy C, Song Y, Ng-Hublin J, Estcourt A, Hijjawi N, et al. Specific and quantitative detection and identification of Cryptosporidium hominis and C. parvum in clinical and environmental samples. Exp Parasitol. 2013;135(1):142–7. doi: 10.1016/j.exppara.2013.06.014 23838581

26. Clark P, Spencer PBS. Description of three new species of Theileria Bettencourt, Franca & Borges, 1907 from Macropodoidea in Western Australia. T Roy Soc South Australia. 2007;131:100–6.

27. Dawood KE, Morgan JA, Busfield F, Srivastava M, Fletcher TI, Sambono J, et al. Observation of a novel Babesia spp. in Eastern Grey Kangaroos (Macropus giganteus) in Australia. Int J Parasitol Parasites Wildl. 2013;2:54–61. doi: 10.1016/j.ijppaw.2012.12.001 24533316

28. Loh SM, Paparini A, Ryan U, Irwin P, Oskam C. Identification of Theileria fuliginosa-like species in Ixodes australiensis ticks from western grey kangaroos (Macropus fuliginosus) in Western Australia. Ticks Tick Borne Dis. 2018;9(3):632–7. doi: 10.1016/j.ttbdis.2018.02.001 29439876

29. Storey-Lewis B, Mitrovic A, McParland B. Molecular detection and characterisation of Babesia and Theileria in Australian hard ticks. Ticks Tick Borne Dis. 2018;9(3):471–8. doi: 10.1016/j.ttbdis.2017.12.012 29331578

30. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80. doi: 10.1093/molbev/mst010 23329690

31. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33(7):1870–4. doi: 10.1093/molbev/msw054 27004904

32. Nei M, Kumar S. Molecular evolution and phylogenetics. Oxford: Oxford University Press; 2000.

33. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10(3):512–26. doi: 10.1093/oxfordjournals.molbev.a040023 8336541

34. Abramoff MD, Magalhaes PJ, Ram SJ. Image processing with image. Biophotonics International. 2004; 11 36–42.

35. Chinnery PF, Howell N, Andrews RM, Turnbull DM. Mitochondrial DNA analysis: polymorphisms and pathogenicity. J Med Genet. 1999;36(7):505–10. 10424809

36. Harris J. Naming no names: Comments on the taxonomy of small piroplasmids in canids. Parasit Vectors. 2016;9:289. doi: 10.1186/s13071-016-1567-5 27193588

37. Uilenberg G. Babesia-A historical overview. Veterinary Parasitology. 2006;138:3–10. doi: 10.1016/j.vetpar.2006.01.035 16513280

38. Greay TL, Zahedi A, Krige AS, Owens JM, Rees RL, Ryan UM, et al. Response to the Letter to the Editor by Harris. Parasit Vectors. 2019;12(1):178. doi: 10.1186/s13071-019-3439-2 31014394

39. Gjerde B, Vikoren T, Hamnes IS. Molecular identification of Sarcocystis halieti n. sp., Sarcocystis lari and Sarcocystis truncata in the intestine of a white-tailed sea eagle (Haliaeetus albicilla) in Norway. Int J Parasitol Parasites Wildl. 2018;7(1):1–11. doi: 10.1016/j.ijppaw.2017.12.001 29270360

40. Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, Wu HW, et al. The synergistic effect of concomitant schistosomiasis, hookworm, and trichuris infections on children's anemia burden. PLoS Neglec Trop D. 2008;2(6).

41. Barbosa AD, Gofton AW, Paparini A, Codello A, Greay T, Gillett A, et al. Increased genetic diversity and prevalence of co-infection with Trypanosoma spp. in koalas (Phascolarctos cinereus) and their ticks identified using next-generation sequencing (NGS). PLoS One. 2017;12(7).

42. Roberts FHS. Australian ticks. In: Organization CSaIR, editor. Melbourne1970.

43. Knowles DP, Kappmeyer LS, Haney D, Herndon DR, Fry LM, Munro JB, et al. Discovery of a novel species, Theileria haneyi n. sp., infective to equids, highlights exceptional genomic diversity within the genus Theileria: implications for apicomplexan parasite surveillance. Int J Parasitol. 2018;48(9–10):679–90. doi: 10.1016/j.ijpara.2018.03.010 29885436

44. Donahoe SL, Peacock CS, Choo AY, Cook RW, O'Donoghue P, Crameri S, et al. A retrospective study of Babesia macropus associated with morbidity and mortality in eastern grey kangaroos (Macropus giganteus) and agile wallabies (Macropus agilis). Int J Parasitol Parasites Wildl. 2015;4(2):268–76. doi: 10.1016/j.ijppaw.2015.02.002 26106576

45. Mackerras MJ. The haematozoa of Australian mammals. Aust J Zool. 1959;7:105–35.


Článek vyšel v časopise

PLOS One


2019 Číslo 12