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The host-specificity of Theileria sp. (sable) and Theileria sp. (sable-like) in African Bovidae and detection of novel Theileria in antelope and giraffe

Published online by Cambridge University Press:  30 September 2019

Ronel Pienaar ,
Antoinette Josemans ,
Abdalla A. Latif  and
Ben J. Mans Open the ORCID record for Ben J. Mans [Opens in a new window]
Ronel Pienaar
Affiliation:
Epidemiology, Parasites and Vectors, Agricultural Research Council-Onderstepoort Veterinary Research, Onderstepoort 0110, South Africa
Antoinette Josemans
Affiliation:
Epidemiology, Parasites and Vectors, Agricultural Research Council-Onderstepoort Veterinary Research, Onderstepoort 0110, South Africa
Abdalla A. Latif
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, Durban, Westville, South Africa
Ben J. Mans*
Affiliation:
Epidemiology, Parasites and Vectors, Agricultural Research Council-Onderstepoort Veterinary Research, Onderstepoort 0110, South Africa The Department of Veterinary Tropical Diseases, University of Pretoria, Pretoria, South Africa Department of Life and Consumer Sciences, University of South Africa, Pretoria, South Africa
*
Author for correspondence: Ben J. Mans, E-mail: [email protected]
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Abstract

Tick-borne diseases caused by Theileria are of economic importance in domestic and wildlife ruminants. The majority of Theileria infects a limited number of host species, supporting the concept of host specificity. However, some Theileria seem to be generalists challenging the host specificity paradigm, such as Theileria sp. (sable) reported from various vertebrate hosts, including African buffalo, cattle, dogs and different antelope species. We tested the hypothesis that T. sp. (sable) uses Bovidae as hosts in general using a real-time polymerase chain reaction assay specific for T. sp. (sable) and a closely related genotype: T. sp. (sable-like). Various antelope species from the Tragelaphini (black wildebeest, blesbuck, blue wildebeest, gemsbuck, sable and waterbuck) tested positive for either T. sp. (sable) or T. sp. (sable-like). However, no African buffalo (n = 238) or cattle (n = 428) sampled in the current study tested positive, suggesting that these latter species are not carrier hosts. The results were confirmed using next-generation sequencing which also indicated at least 13 new genotypes or species found in various antelope and giraffes. Genotypes were found in single host species or in evolutionarily related hosts, suggesting that host specificity in Theileria may be a lineage specific phenomenon likely associated with tick-host-parasite co-evolution.

Keywords

Bovidaenext-generation sequencingreal-time PCRTheileria sp. (sable)Theileria sp. (sable-like)
Type
Research Article
Information
Parasitology , Volume 147 , Issue 2 , February 2020 , pp. 213 - 224
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Copyright
Copyright © Cambridge University Press 2019

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References

Adamu, M, Troskie, M, Oshadu, DO, Malatji, DP, Penzhorn, BL and Matjila, PT (2014) Occurrence of tick-transmitted pathogens in dogs in Jos, Plateau State, Nigeria. Parasites & Vectors 7, 119.CrossRefGoogle ScholarPubMed
Allsopp, BA, Baylis, HA, Allsopp, MTPE, Cavalier-Smith, T, Bishop, RP, Carrington, DM, Sohanpal, B and Spooner, P (1993) Discrimination between six species of Theileria using oligonucleotide probes which detect small subunit ribosomal RNA sequences. Parasitology 107, 157–165.CrossRefGoogle ScholarPubMed
Altay, K, Dumanli, N and Aktas, M (2007) Molecular identification, genetic diversity and distribution of Theileria and Babesia species infecting small ruminants. Veterinary Parasitology 147, 161–165.CrossRefGoogle ScholarPubMed
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Ansell, WFH (1971) Order artiodactyla. In Meester, J and Setzer, HW (eds), The Mammals of Africa: an Identification Manual. Washington, DC: Smithsonian Institution Press, pp. 15–83.Google Scholar
Aydin, MF, Aktas, M and Dumanli, N (2015) Molecular identification of Theileria and Babesia in ticks collected from sheep and goats in the Black Sea region of Turkey. Parasitology Research 114, 65–69.CrossRefGoogle ScholarPubMed
Berggoetz, M, Schmid, M, Ston, D, Wyss, V, Chevillon, C, Pretorius, AM and Gern, L (2014) Tick-borne pathogens in the blood of wild and domestic ungulates in South Africa: interplay of game and livestock. Ticks and Tick Borne Diseases 5, 166–175.CrossRefGoogle ScholarPubMed
Bigalke, RD, Keep, ME and Schoeman, JH (1972) Some protozoan parasites of tragelaphine antelopes in South Africa with special reference to a Babesia sp. in a bushbuck and a Trypanosoma theileri-like parasite in a nyala. Onderstepoort Journal of Veterinary Research 39, 225–228.Google Scholar
Bishop, R, Musoke, A, Morzaria, S, Gardner, M and Nene, V (2004) Theileria: intracellular protozoan parasites of wild and domestic ruminants transmitted by ixodid ticks. Parasitology 129, S271–S283.CrossRefGoogle ScholarPubMed
Bishop, RP, Odongo, DO, Dolan, TT, Dolan, RB, Skilton, RA and Sayer, PD (2019) Theileriosis in mountain bongo repatriated to Kenya: a clinical and molecular investigation. Journal of Zoo and Wildlife Medicine 50, 342–349.Google ScholarPubMed
Brothers, PS, Collins, NE, Oosthuizen, MC, Bhoora, R, Troskie, M and Penzhorn, BL (2011) Occurrence of blood-borne tick-transmitted parasites in common tsessebe (Damaliscus lunatus) antelope in Northern Cape Province, South Africa. Veterinary Parasitology 183, 160–165.CrossRefGoogle ScholarPubMed
Chaisi, ME, Sibeko, KP, Collins, NE, Potgieter, FT and Oosthuizen, MC (2011) Identification of Theileria parva and Theileria sp. (buffalo) 18S rRNA gene sequence variants in the African Buffalo (Syncerus caffer) in Southern Africa. Veterinary Parasitology 182, 150–162.CrossRefGoogle Scholar
Chaisi, ME, Janssens, ME, Vermeiren, L, Oosthuizen, MC, Collins, NE and Geysen, D (2013) Evaluation of a real-time PCR test for the detection and discrimination of Theileria species in the African buffalo (Syncerus caffer). PLoS ONE 8, e75827.CrossRefGoogle Scholar
Chaisi, ME, Collins, NE and Oosthuizen, MC (2014) Phylogeny of Theileria buffeli genotypes identified in the South African buffalo (Syncerus caffer) population. Veterinary Parasitology 204, 87–95.CrossRefGoogle ScholarPubMed
Chaligiannis, Ι, Fernández de Mera, IG, Papa, A, Sotiraki, S and de la Fuente, J (2018) Molecular identification of tick-borne pathogens in ticks collected from dogs and small ruminants from Greece. Experimental and Applied Acarology 74, 443–453.CrossRefGoogle Scholar
Eygelaar, D, Jori, F, Mokopasetso, M, Sibeko, KP, Collins, NE, Vorster, I, Troskie, M and Oosthuizen, MC (2015) Tick-borne haemoparasites in African buffalo (Syncerus caffer) from two wildlife areas in Northern Botswana. Parasites & Vectors 8, 26.CrossRefGoogle ScholarPubMed
García-Sanmartín, J, Aurtenetxe, O, Barral, M, Marco, I, Lavin, S, García-Pérez, AL and Hurtado, A (2007) Molecular detection and characterization of piroplasms infecting cervids and chamois in Northern Spain. Parasitology 134, 391–398.CrossRefGoogle ScholarPubMed
Garner, BC, Holman, P and Berent, LM (2012) Theileriosis in a reindeer (Rangifer tarandus tarandus) associated with a potentially novel Theileria sp. Veterinary Clinical Pathology 41, 497–501.CrossRefGoogle Scholar
Gentry, AW (1992) The subfamilies and tribes of the family Bovidae. Mammal Review 22, 1–32.CrossRefGoogle Scholar
Githaka, N, Konnai, S, Skilton, R, Kariuki, E, Kanduma, E, Murata, S and Ohashi, K (2013) Genotypic variations in field isolates of Theileria species infecting giraffes (Giraffa camelopardalis tippelskirchi and Giraffa camelopardalis reticulata) in Kenya. Parasitology International 62, 448–453.CrossRefGoogle Scholar
Grootenhuis, JG, Young, AS, Kimber, CD and Drevemo, SA (1975) Investigations on a Theileria species from an impala. Journal of Wildlife Diseases 11, 122–127.CrossRefGoogle ScholarPubMed
Hassanin, A, Delsuc, F, Ropiquet, A, Hammere, C, Jansen van Vuuren, B, Matthee, C, Ruiz-Garcia, M, Catzefli, F, Areskoug, V, Thanh Nguyen, T and Couloux, A (2012) Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. Comptes Rendus Biologies 335, 32–50.CrossRefGoogle Scholar
Iqbal, F, Khattak, R, Ozubek, S, Khattak, M, Rasul, A and Aktas, M (2013) Application of the reverse line blot assay for the molecular detection of Theileria and Babesia sp. in sheep and goat blood samples from Pakistan. Iran Journal of Parasitology 8, 289–295.Google ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Mans, BJ, Pienaar, R, Latif, AA and Potgieter, FT (2011) Diversity in the 18S SSU rRNA V4 hyper-variable region of Theileria in bovines and African buffalo (Syncerus caffer) from Southern Africa. Parasitology 138, 766–779.CrossRefGoogle Scholar
Mans, BJ, Pienaar, R and Latif, AA (2015) A review of Theileria diagnostics and epidemiology. International Journal of Parasitology: Parasites and Wildlife 4, 104–118.Google ScholarPubMed
Mans, BJ, Pienaar, R, Ratabane, J, Pule, B and Latif, AA (2016) Investigating the diversity of the 18S SSU rRNA hyper-variable region of Theileria in cattle and Cape buffalo (Syncerus caffer) from Southern Africa using a next generation sequencing approach. Ticks and Tick-borne Diseases 7, 869–879.CrossRefGoogle ScholarPubMed
Matjila, PT, Leisewitz, AL, Oosthuizen, MC, Jongejan, F and Penzhorn, BL (2008) Detection of a Theileria species in dogs in South Africa. Veterinary Parasitology 157, 34–40.CrossRefGoogle ScholarPubMed
Matthee, CA and Davis, SK (2001) Molecular insights into the evolution of the family Bovidae: a nuclear DNA perspective. Molecular Biology and Evolution 18, 1220–1230.CrossRefGoogle ScholarPubMed
Muhanguzi, D, Matovu, E and Waiswa, C (2010) Prevalence and characterization of Theileria and Babesia species in cattle under different husbandry systems in Western Uganda. International Journal of Animal Veterinary Advances 2, 51–58.Google Scholar
Neitz, WO (1931) Blood parasites of game in Zululand. Preliminary report. 17th Report of the Director of Veterinary Service and Animal Industry, Union of South Africa, pp. 45–60.Google Scholar
Nijhof, AM, Penzhorn, BL, Lynen, G, Mollel, JO, Morkel, P, Bekker, CP and Jongejan, F (2003) Babesia bicornis sp. nov. and Theileria bicornis sp. nov.: tick-borne parasites associated with mortality in the black rhinoceros (Diceros bicornis). Journal of Clinical Microbiology 41, 2249–2254.CrossRefGoogle Scholar
Nijhof, AM, Pillay, V, Steyl, J, Prozesky, L, Stoltsz, WH, Lawrence, JA, Penzhorn, BL and Jongejan, F (2005) Molecular characterization of Theileria species associated with mortality in four species of African antelopes. Journal of Clinical Microbiology 43, 5907–5911.CrossRefGoogle ScholarPubMed
Njiiri, NE, Bronsvoort, BM, Collins, NE, Steyn, HC, Troskie, M, Vorster, I, Thumbi, SM, Sibeko, KP, Jennings, A, van Wyk, IC, Mbole-Kariuki, M, Kiara, H, Poole, EJ, Hanotte, O, Coetzer, K, Oosthuizen, MC, Woolhouse, M and Toye, P (2015) The epidemiology of tick-borne haemoparasites as determined by the reverse line blot hybridization assay in an intensively studied cohort of calves in western Kenya. Veterinary Parasitology 210, 69–76.CrossRefGoogle Scholar
Oosthuizen, MC, Zweygarth, E, Collins, NE, Troskie, M and Penzhorn, BL (2008) Identification of a novel Babesia sp. from a sable antelope (Hippotragus niger Harris, 1838). Journal of Clinical Microbiology 46, 2247–2251.CrossRefGoogle Scholar
Oosthuizen, MC, Allsopp, BA, Troskie, M, Collins, NE and Penzhorn, BL (2009) Identification of novel Babesia and Theileria species in South African giraffe (Giraffa camelopardalis, Linnaeus, 1758) and roan antelope (Hippotragus equinus, Desmarest 1804). Veterinary Parasitology 163, 39–46.CrossRefGoogle Scholar
Oura, CA, Tait, A, Asiimwe, B, Lubega, GW and Weir, W (2011) Theileria parva genetic diversity and haemoparasite prevalence in cattle and wildlife in and around Lake Mburo National Park in Uganda. Parasitology Research 108, 1365–1374.CrossRefGoogle ScholarPubMed
Ozubek, S and Aktas, M (2017) Molecular and parasitological survey of ovine piroplasmosis, including the first report of Theileria annulata (Apicomplexa: Theileridae) in sheep and goats from Turkey. Journal of Medical Entomology 54, 212–220.CrossRefGoogle ScholarPubMed
Papli, N, Landt, O, Fleischer, C, Koekemoer, JO, Mans, BJ, Pienaar, R, Josemans, A, Zweygarth, E, Potgieter, F and Latif, AA (2011) Evaluation of a TaqMan real-time PCR for the detection of Theileria parva in buffalo and cattle. Veterinary Parasitology 175, 356–359.CrossRefGoogle ScholarPubMed
Pfaffl, MW (2004) Quantification strategies in real-time PCR. In Bustin, SA (ed.), A-Z of Quantitative PCR. La Jolla, CA, USA: International University Line (IUL), pp. 87–112.Google Scholar
Pfitzer, S, Oosthuizen, MC, Bosman, AM, Vorster, I and Penzhorn, BL (2011) Tick-borne blood parasites in nyala (Tragelaphus angasii Gray 1849) from KwaZulu-Natal, South Africa. Veterinary Parasitology 176, 126–131.CrossRefGoogle ScholarPubMed
Pienaar, R, Potgieter, FT, Latif, AA, Thekisoe, OMM and Mans, BJ (2011a) Mixed Theileria infections in free-ranging buffalo herds: implications for diagnosing Theileria parva infections in Cape buffalo (Syncerus caffer). Parasitology 138, 884–895.CrossRefGoogle Scholar
Pienaar, R, Potgieter, FT, Latif, AA, Thekisoe, OMM and Mans, BJ (2011b) The Hybrid II assay: a sensitive and specific real-time hybridization assay for the diagnosis of Theileria parva infection in Cape buffalo (Syncerus caffer) and cattle. Parasitology 138, 884–895.CrossRefGoogle Scholar
Pienaar, R, Potgieter, FT, Latif, AA, Thekisoe, OMM and Mans, BJ (2014) Geographic distribution of Theileria sp. (buffalo) and Theileria sp. (bougasvlei) in Cape buffalo (Syncerus caffer) in Southern Africa: implications for speciation. Parasitology 141, 411–424.CrossRefGoogle Scholar
Pienaar, R, Latif, AA and Mans, BJ (2018) Investigations into the host specificity of Theileria taurotragi. Veterinary Parasitology 254, 30–35.CrossRefGoogle ScholarPubMed
Sibeko, KP, Oosthuizen, MC, Collins, NE, Geysen, D, Rambritch, NE, Latif, AA, Groeneveld, HT, Potgieter, FT and Coetzer, JA (2008) Development and evaluation of a real-time polymerase chain reaction test for the detection of Theileria parva infections in Cape buffalo (Syncerus caffer) and cattle. Veterinary Parasitology 155, 37–48.CrossRefGoogle ScholarPubMed
Spitalska, E, Riddell, M, Heyne, H and Sparagano, OA (2005) Prevalence of theileriosis in Red Hartebeest (Alcelaphus buselaphus caama) in Namibia. Parasitology Research 97, 77–79.CrossRefGoogle Scholar
Steyl, JC, Prozesky, L, Stoltsz, WH and Lawrence, JA (2012) Theileriosis (Cytauxzoonosis) in Roan antelope (Hippotragus equinus): field exposure to infection and identification of potential vectors. Onderstepoort Journal of Veterinary Research 79, E1–E8.CrossRefGoogle ScholarPubMed
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Tembo, S, Collins, NE, Sibeko-Matjila, KP, Troskie, M, Vorster, I, Byaruhanga, C and Oosthuizen, MC (2018) Occurrence of tick-borne haemoparasites in cattle in the Mungwi District, Northern Province, Zambia. Ticks and Tick Borne Diseases 9, 707–717.CrossRefGoogle ScholarPubMed
Torina, A, Vicente, J, Alongi, A, Scimeca, S, Turlá, R, Nicosia, S, Di Marco, V, Caracappa, S and de la Fuente, J (2007) Observed prevalence of tick-borne pathogens in domestic animals in Sicily, Italy during 2003–2005. Zoonoses and Public Health 54, 8–15.CrossRefGoogle ScholarPubMed
Vrba, ES (1979) Phylogenetic analysis and classification of fossil and recent Alcelaphini Mammalia: Bovidae. Biological Journal of the Linnean Society 11, 207–228.CrossRefGoogle Scholar
Walker, JB, Keirans, JE and Horak, IG (2000) The Genus Rhipicephalus (Acari, Ixodidae): a Guide to the Brown Ticks of the World. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Wilson, DE, Bartsch, RC, Bigalke, RD and Thomas, SE (1974) Observations on mortality rates and disease in roan and sable antelope on nature reserves in the Transvaal. South African Journal of Wildlife Research 4, 203–206.Google Scholar
Yusufmia, SB, Collins, NE, Nkuna, R, Troskie, M, Van den Bossche, P and Penzhorn, BL (2010) Occurrence of Theileria parva and other haemoprotozoa in cattle at the edge of Hluhluwe-iMfolozi Park KwaZulu-Natal, South Africa. Journal of the South African Veterinary Association 81, 45–49.CrossRefGoogle ScholarPubMed
Zhang, Y, Li, T, Cui, Y, Wang, J, Lv, Y, Wang, R, Jian, F, Zhang, L, Wang, J, Yang, G and Ning, C (2016) The first report of Anaplasma phagocytophilum and a novel Theileria spp. co-infection in a South African giraffe. Parasitology International 65, 347–351.CrossRefGoogle Scholar
Zweygarth, E, Benade, J, Steyl, J, Prozesky, L, Koekemoer, O and Josemans, AI (2009) In vitro cultivation of a Theileria species from a roan antelope (Hippotragus equinus). Parasitology Research 105, 1755–1757.CrossRefGoogle Scholar
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