Morphological polymorphism of Trypanosoma copemani and description of the genetically diverse T. vegrandis sp. nov. from the critically endangered Australian potoroid, the brush-tailed bettong (Bettongia penicillata (Gray, 1837))

Particle and Fibre Toxicology

RC Andrew Thompson³  Alan J Lymbery²  Stephanie S Godfrey³  Adrian F Wayne¹  Adriana Botero³  Craig K Thompson³ 

[1] Science Division, Department of Environment and Conservation, Manjimup, WA 6258, Australia;Fish Health Unit and Freshwater Fish Group, School of Veterinary and Life Sciences, Murdoch University, South Street, Western Australia, 6150, Australia;School of Veterinary and Life Sciences, Murdoch University, South Street, Western Australia, 6150, Australia

关键词: penicillata;    Bettongia;    Woylie;    Fluorescence;    Sequencing;    PCR;    Morphology;    T. copemani;    Trypanosoma vegrandis;   

Others  :  1227979
DOI  :  10.1186/1756-3305-6-121

 received in 2013-02-26, accepted in 2013-04-22,  发布年份 2013

【 摘 要 】

Background

The trypanosome diversity of the Brush-tailed Bettong (Bettongia penicillata), known locally as the woylie, has been further investigated. At a species level, woylies are critically endangered and have declined by 90% since 1999. The predation of individuals made more vulnerable by disease is thought to be the primary cause of this decline, but remains to be proven.

Methods

Woylies were sampled from three locations in southern Western Australia. Blood samples were collected and analysed using fluorescence in situ hybridization, conventional staining techniques and microscopy. Molecular techniques were also used to confirm morphological observations.

Results

The trypanosomes in the blood of woylies were grouped into three morphologically distinct trypomastigote forms, encompassing two separate species. The larger of the two species, Trypanosoma copemani exhibited polymorphic trypomastigote forms, with morphological phenotypes being distinguishable, primarily by the distance between the kinetoplast and nucleus. The second trypanosome species was only 20% of the length of T. copemani and is believed to be one of the smallest recorded trypanosome species from mammals. No morphological polymorphism was identified for this genetically diverse second species. We described the trypomastigote morphology of this new, smaller species from the peripheral blood of the woylie and proposed the name T. vegrandis sp. nov. Temporal results indicate that during T. copemani Phenotype 1 infections, the blood forms remain numerous and are continuously detectable by molecular methodology. In contrast, the trypomastigote forms of T. copemani Phenotype 2 appear to decrease in prevalence in the blood to below molecular detectable levels.

Conclusions

Here we report for the first time on the morphological diversity of trypanosomes infecting the woylie and provide the first visual evidence of a mixed infection of both T. vegrandis sp. nov and T. copemani. We also provide supporting evidence that over time, the intracellular T. copemani Phenotype 2 may become localised in the tissues of woylies as the infection progresses from the active acute to chronic phase. As evidence grows, further research will be necessary to investigate whether the morphologically diverse trypanosomes of woylies have impacted on the health of their hosts during recent population declines.

【 授权许可】

   
2013 Thompson et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Barrett MP, Burchmore RJS, Stich A, Lazzari JO, Frasch AC, Cazzulo JJ, Krishna S: The trypanosomiases. Lancet 2003, 362:1469-1480.
• [2]Brun R, Hecker H, Lun ZR: Trypanosoma evansi and T. equiperdum: distribution, biology, treatment and phylogenetic relationship (a review). Vet Parasitol 1998, 79:95-107.
• [3]D’Archivio S, Medina M, Cosson A, Chamond N, Rotureau B, Minoprio P, Goyard S: Genetic engineering of Trypanosoma (Dutonella) vivax and in vitro differentiation under axenic conditions. PLoS Negl Trop Dis 2011, 5:e1461.
• [4]Steverding D: The history of African trypanosomiasis. Parasit Vectors 2008, 1:3. BioMed Central Full Text
• [5]Wyatt KB, Campos PF, Gilbert MTP, Kolokotronis SO, Hynes WH, DeSalle R, Daszak P, MacPhee RDE, Greenwood AD: Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease. PLoS One 2008, 3:1-9.
• [6]Andrews CW: An account of a visit to Christmas Island in 1908. J Zool 1987, 1909(1909):101-103.
• [7]Pickering J, Norris CA: New evidence concerning the extinction of the endemic murid Rattus macleari from Christmas Island, Indian Ocean. Aust Mammal 1996, 19:19-25.
• [8]Averis S, Thompson RCA, Lymbery AJ, Wayne AF, Morris KD, Smith A: The diversity, distribution and host-parasite associations of trypanosomes in Western Australian wildlife. Parasitology 2009, 136:1269-1279.
• [9]Smith A, Clark P, Averis S, Lymbery AJ, Wayne AF, Morris KD, Thompson RCA: Trypanosomes in a declining species of threatened Australian marsupial, the brush-tailed bettong Bettongia penicillata (Marsupialia: Potoroidae). Parasitology 2008, 135:1329-1335.
• [10]De Tores PJ, Start AN: Brush-tailed Bettong (Bettongia penicillata). In The Mammals of Australia. Edited by Van Dyck S, Strahan RJ. Sydney: Reed New Holland; 2008:291-292.
• [11]Wayne AF: Diagnosis of recent woylie (Bettongia penicillata ogilbyi) declines in southwestern Australia: Progress Report of the Woylie Conservation Research Project. Perth: Western Australia Government Department of Environment and Conservation; 2008.
• [12]Claridge AW, Seebeck JH, Rose R: Bettongs, Potoroos and the Musky Rat-Kangaroo. Melbourne: CSIRO Publishing; 2007.
• [13]Pacioni C, Wayne AF, Spencer PBS: Effects of habitat fragmentation on population structure and long distance gene flow in an endangered marsupial: the woylie. J Zool 1987, 283:98-107.
• [14]Abbott I: Historical perspectives of the ecology of some conspicuous vertebrate species in south-west Western Australia. Conserv Sci W Aust 2008, 6:1-214.
• [15]Bettongia penicillata ogilbyi in Species Profile and Threats Database. http://www.environment.gov.au/cgi-bin/sprat/public/publicspecies.pl?taxon_id=66844 webcite
• [16]Wayne AF, Maxwell M, Ward C, Vellios C, Ward B, Liddelow GL, Wilson I, Wayne JC, Williams MR: The importance of getting the numbers right: quantifying the rapid and substantial decline of an abundant marsupial, Bettongia penicillata. Wildl Resin press
• [17]Wayne A, Maxwell M, Nicholls P, Pacioni C, Reiss A, Smith A, Thompson RCA, Vellios C, Ward C, Wayne J: The Woylie Conservation Research Project: investigating the cause(s) of woylie declines in the Upper Warren region. Perth: Western Australia Government Department of Environment and Conservation; 2011.
• [18]Groom C: Justification for continued conservation efforts following the delisting of a threatened species: a case study of the woylie, Bettongia penicillata ogilbyi (Marsupialia : Potoroidae). Wildl Res 2010, 37:183-193.
• [19]Botero A, Thompson CK, Peacock C, Clode PL, Nicholls PK, Wayne AF, Lymbery AJ, Thompson RCA: Trypanosomes genetic diversity, polyparasitism and the population decline of the critically endangered Australian marsupial, the brush tailed bettong or woylie (Bettongia penicillata). Int J Parasitol Parasites Wildl 2013, 2:77-89.
• [20]Li A: Role of feral pig (Sus scrofa) in the dissemination of Phytophthora cinnamomi in South-western Australia. Murdoch University: PhD Thesis; 2012.
• [21]Hoare CA: The trypanosomes of mammals. Oxford, England: Blackwell Scientific Publishing; 1972.
• [22]JMP 10.0 SAS. Carey, NC: Institute Inc;
• [23]McInnes LM, Gillett A, Hanger J, Reid SA, Ryan UM: The potential impact of native Australian trypanosome infections on the health of koalas (Phascolarctos cinereus). Parasitology 2011, 138:1-11.
• [24]Austen JM, Jefferies R, Friend JA, Ryan U, Adams P, Reid SA: Morphological and molecular characterization of Trypanosoma copemani n. sp. (Trypanosomatidae) isolated from Gilbert’s potoroo (Potorous gilbertii) and quokka (Setonix brachyurus). Parasitology 2009, 136:783-792.
• [25]Teixeira ARL, Nascimento RJ, Sturm NR: Evolution and pathology in Chagas disease: a review. Mem Inst Oswaldo Cruz 2006, 101:463-491.
• [26]McInnes LM, Hanger J, Simmons G, Reid SA, Ryan UM: Novel trypanosome Trypanosoma gilletti sp. (Euglenozoa: Trypanosomatidae) and the extension of the host range of Trypanosoma copemani to include the koala (Phascolarctos cinereus). Parasitology 2011, 138:59-70.
• [27]Paparini A, Irwin PJ, Warren K, McInnes LM, De Tores P, Ryan UM: Identification of novel trypanosome genotypes in native Australian marsupials. Vet Parasitol 2011, 183:21-30.
• [28]McInnes LM, Gillett A, Ryan UM, Austen J, Campbell RS, Hanger J, Reid SA: Trypanosoma irwini n. sp (Sarcomastigophora: Trypanosomatidae) from the koala (Phascolarctos cinereus). Parasitology 2009, 136:875-885.
• [29]Hamilton PB, Stevens JR, Holz P, Boag B, Cooke B, Gibson WC: The inadvertent introduction into Australia of Trypanosoma nabiasi, the trypanosome of the European rabbit (Oryctolagus cuniculus), and its potential for biocontrol. Mol Ecol 2005, 14:3167-3175.
• [30]Hatama S, Shibahara T, Suzuki M, Kadota K, Uchida I, Kanno T: Isolation of a Megatrypanum trypanosome from sika deer (Cervus nippon yesoensis) in Japan. Vet Parasitol 2007, 149:56-64.
• [31]Riedel D: Reproduction, Structure and Host Specificity of Trypanosoma (Herpetosoma) tamiasi sp. n. from the Eastern Chipmunk, Tamias striatus. J Eukaryot Microbiol 1975, 22:8-17.
• [32]Karbowiak G, Wita I: Trypanosoma (Herpetosoma) grosi kosewiense subsp. n., the parasite of the yellow-necked mouse Apodemus flavicollis (Melchior, 1834). Acta Protozool 2004, 43:173-178.
• [33]Sato H, Al-Adhami BH, Une Y, Kamiya H: Trypanosoma (Herpetosoma) kuseli sp. n. (Protozoa: Kinetoplastida) in Siberian flying squirrels (Pteromys volans). Parasitol Res 2007, 101:453-461.
• [34]Upton SJ, Fridell RA, Tilley M: Trypanosoma kansasensis sp. n. from Neotoma floridana in Kansas. J Wildl Dis 1989, 25:410-412.
• [35]Kingston N, Morton JK: Trypanosoma cervi sp. n. from elk (Cervus canadensis) in Wyoming. J Parasitol 1975, 61:17-23.
• [36]Madeira MF, Sousa MA, Barros JHS, Figueiredo FB, Fagundes A, Schubach A, De Paula CC, Faissal BNS, Fonseca TS, Thoma HK: Trypanosoma caninum n. sp.(Protozoa: Kinetoplastida) isolated from intact skin of a domestic dog (Canis familiaris) captured in Rio de Janeiro, Brazil. Parasitology 2009, 136:411-423.
• [37]Bettiol SS, Jakes K, Le DD, Goldsmid JM, Hocking G: First Record of Trypanosomes in Tasmanian Bandicoots. J Parasitol 1998, 84:538-541.