Diversity in the 18S SSU rRNA V4 hyper-variable region of Theileria spp. in Cape buffalo (Syncerus caffer) and cattle from southern Africa

Parasitology

Volumn 138, Issue 6, 2011, Pages 766-779

  Mans, Ben J ^a,b   Pienaar, Ronel ^a   Latif, Abdalla A ^a,b   Potgieter, Fred T ^a  

^a ONDERSTEPOORT VETERINARY INSTITUTE   (South Africa)

^b UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

18S SSU; diversity; species; Theileria; Theileria parva

Indexed keywords

GENOMIC DNA; MOLECULAR MARKER; PROTOZOAL DNA; PROTOZOAL RNA; RNA 18S; SMALL SUBUNIT RIBOSOMAL RNA;

18S GENE; ARTICLE; BUFFALO; CATTLE; CLADISTICS; CONTROLLED STUDY; DNA POLYMORPHISM; GENE; GENE SEQUENCE; GENETIC DISTANCE; GENETIC VARIABILITY; GENOTYPE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; S5 GENE; SEQUENCE ALIGNMENT; SOUTH AFRICA; SPECIES DIFFERENTIATION; SPECIES DIVERSITY; SYNCERUS CAFFER; THEILERIA; THEILERIA BUFFELI; THEILERIA MUTANS; THEILERIA PARVA; THEILERIA TAUROTRAGI; THEILERIA VELIFERA;

AFRICA, SOUTHERN; ANIMALS; BASE SEQUENCE; BUFFALOES; CATTLE; CATTLE DISEASES; GENETIC VARIATION; GENOTYPE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RIBOSOMAL PROTEINS; RNA, RIBOSOMAL, 18S; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; THEILERIA; THEILERIASIS;

BOS; BOVINAE; SYNCERUS CAFFER; SYNCERUS CAFFER CAFFER; THEILERIA; THEILERIA BUFFELI; THEILERIA MUTANS; THEILERIA PARVA; THEILERIA SP.; THEILERIA TAUROTRAGI; THEILERIA VELIFERA;

EID: 79955995579     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011000187     Document Type: Article

References (65)

1. Allsopp, B. A., Baylis, H. A., Allsopp, M. T. P. E., Cavalier-Smith, T., Bishop, R. P., Carrington, D. M., 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. (Pubitemid 23233492)
2. Allsopp, B., Carrington, M., Baylis, H., Sohal, S., Dolan, T. and Iams,K. (1989). Improved characterization of Theileria parva isolates using the polymerase chain reaction and oligonucleotide probes. Molecular and Biochemical Parasitology 35, 137-147.
3. Allsopp, M. T., Cavalier-Smith, T., De Waal, D. T. and Allsopp, B. A. (1994). Phylogeny and evolution of the piroplasms. Parasitology 108, 147-152. (Pubitemid 24056822)
4. Allsopp, M. T., Theron, J., Coetzee, M. L., Dunsterville, M. T. and Allsopp, B. A. (1999). The occurrence of Theileria and Cowdria parasites in African buffalo (Syncerus caffer) and their associated Amblyomma hebraeum ticks. Onderstepoort Journal of Veterinary Research 66, 245-249. (Pubitemid 129721910)
5. 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. (Pubitemid 46770981)
6. Barnett, S. F. (1977). Theileria. In Parasitic Protozoa, Vol. IV (ed. Kreier, J. P.), pp. 77-113. Academic Press, New York, USA.
7. Bhoora, R., Franssen, L., Oosthuizen, M. C., Guthrie, A. J., Zweygarth, E., Penzhorn, B. L., Jongejan, F. and Collins, N. E. (2009). Sequence heterogeneity in the 18S rRNA gene within Theileria equi and Babesia caballi from horses in South Africa. Veterinary Parasitology 159, 112-120.
8. Brocklesby, D.W. (1962). Cytauxzoon taurotragi Martin and Brocklesby, 1960, a piroplasm of the eland (Taurotragus oryx pattersonianus Lydekker, 1906). Research in Veterinary Science 3, 334-344.
9. Chae, J. S., Allsopp, B. A., Waghela, S. D., Park, J. H., Kakuda, T., Sugimoto, C., Allsopp, M. T., Wagner, G. G. and Holman, P. J. (1999). A study of the systematics of Theileria spp. based upon small-subunit ribosomal RNA gene sequences. Parasitology Research 85, 877-883. (Pubitemid 29467936)
10. Chansiri, K., Kawazu, S., Kamio, T., Terada, Y., Fujisaki, K., Philippe, H. and Sarataphan, N. (1999). Molecular phylogenetic studies on Theileria parasites based on small subunit ribosomal RNA gene sequences. Veterinary Parasitology 83, 99-105. (Pubitemid 29257967)
11. Collins, N. E. and Allsopp, B. A. (1999). Theileria parva ribosomal internal transcribed spacer sequences exhibit extensive polymorphism and mosaic evolution: application to the characterization of parasites from cattle and buffalo. Parasitology 118, 541-551. (Pubitemid 29322099)
12. Conrad, P. A., ole-MoiYoi, O. K., Baldwin, C. L., Dolan, T. T., O'Callaghan, C. J., Njamunggeh, R. E., Grootenhuis, J. G., Stagg, D. A., Leitch, B. L. and Young, A. S. (1989). Characterization of buffalo-derived theilerial parasites with monoclonal antibodies and DNA probes. Parasitology 98, 179-188.
13. Conrad, P. A., Stagg, D. A., Grootenhuis, J. G., Irvin, A. D., Newson, J., Njamunggeh, R. E., Rossiter, P. B. and Young, A. S. (1987). Isolation of Theileria parasites from African buffalo (Syncerus caffer) and characterization with anti-schizont monoclonal antibodies. Parasitology 94, 413-423.
14. Coyne, J. A. and Orr, H. A. (2004). Speciation. Sinauer Associates, Inc. Sunderland, MA, USA.
15. Criado-Fornelio, A., Gónzalez-del-Río, M. A., Buling-Saraña, A. and Barba-Carretero, J. C. (2004). The "expanding universe" of piroplasms. Veterinary Parasitology 119, 337-345.
16. Criado, A., Martinez, J., Buling, A., Barba, J. C., Merino, S., Jefferies, R. and Irwin, P. J. (2006). New data on epizootiology and genetics of piroplasms based on sequences of small ribosomal subunit and cytochrome b genes. Veterinary Parasitology 142, 238-247. (Pubitemid 44750386)
17. De Vos, A. J. and Roos, J. A. (1981). Observations on the transmission of Theileria mutans in South Africa. Onderstepoort Journal of Veterinary Research 48, 1-6.
18. Dschunkowsky, E. and Luhs, J. (1904). Die piroplasmosen der rinder. Centralblatt für Bakteriologie und Parasitenkunde und Infektion und Hygiene 35, 486-493.
19. Eickbush, T. H. and Eickbush, D. G. (2007). Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175, 477-485. (Pubitemid 46798252)
20. Gardner, M. J., Bishop, R., Shah, T., de Villiers, E. P., Carlton, J. M., Hall, N., Ren, Q., Paulsen, I. T., Pain, A., Berriman, M., Wilson, R. J., Sato, S., Ralph, S. A., Mann, D. J., Xiong, Z., Shallom, S. J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A. R., Wasawo, D., Crabtree, J., Wortman, J. R., Haas, B., Angiuoli, S. V., Creasy, T. H., Lu, C., Suh, B., Silva, J. C., Utterback, T. R., Feldblyum, T. V., Pertea, M., Allen, J., Nierman, W. C., Taracha, E. L., Salzberg, S. L., White, O. R., Fitzhugh, H. A., Morzaria, S., Venter, J. C., Fraser, C. M. and Nene, V. (2005). Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309, 134-137. (Pubitemid 40934992)
21. Gubbels, J. M., de Vos, A. P., van der Weide, M., Viseras, J., Schouls, L. M., de Vries, E. and Jongejan, F. (1999). Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. Journal of Clinical Microbiology 37, 1782-1789. (Pubitemid 29235223)
22. Gubbels, M. J., Hong, Y., van der Weide, M., Qi, B., Nijman, I. J., Guangyuan, L. and Jongejan, F. (2000). Molecular characterisation of the Theileria buffeli/orientalis group. International Journal for Parasitology 30, 943-952. (Pubitemid 30601733)
23. Gunderson, J. H., Sogin, M. L., Wollett, G., Hollingdale, M., de la Cruz, V. F., Waters, A. P. and McCutchan, T. F. (1987). Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238, 933-937. (Pubitemid 17163277)
24. Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G. and Gibson, T. J. (1998). Multiple sequence alignment with Clustal X. Trends in Biochemical Science 23, 403-405. (Pubitemid 28511382)
25. Katoh, K. and Toh, H. (2008). Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9, 212.
26. Koch, R. (1903). Interim report on Rhodesian redwater or African Coast Fever. The Journal of Comparative Pathology and Therapeutics 16, 273-280.
27. Lau, A. O. (2009). An overview of the Babesia, Plasmodium and Theileria genomes: A comparative perspective. Molecular and Biochemical Parasitology 164, 1-8.
28. Laughery, J. M., Lau, A. O., White, S. N., Howell, J. M. and Suarez, C. E. (2009). Babesia bovis: Transcriptional analysis of rRNA gene unit expression. Experimental Parasitology 123, 45-50.
29. Lawrence, D. A. (1935). Report of the Director of Veterinary Research, Southern Rhodesia, for the year 1934. Rhodesian Printing and Publishing Co., Salisbury, Rhodesia.
30. Lawrence, J. A. (1979). The differential diagnosis of the bovine theilerias of southern Africa. Journal of the South African Veterinary Association 50, 311-313.
31. Levine, N. D., Corliss, J. O., Cox, F. E., Deroux, G., Grain, J., Honigberg, B. M., Leedale, G. F., Loeblich, A. R. 3rd, Lom, J., Lynn, D., Merinfeld, E. G., Page, F. C., Poljansky, G., Sprague, V., Vavra, J. and Wallace, F. G. (1980). A newly revised classification of the protozoa. Journal of Protozoology 27, 37-58.
32. Martin, H. and Brocklesby, D.W. (1960). A new parasite of the Eland. Veterinary Record 72, 331-332.
33. Matjila, P. T., Leisewitz, A. L., Jongejan, F., Bertschinger, H. J. and Penzhorn, B. L. (2008). Molecular detection of Babesia rossi and Hepatozoon sp. in African wild dogs (Lycaon pictus) in South Africa. Veterinary Parasitology 157, 123-127.
34. Matjila, P. T., Penzhorn, B. L., Bekker, C. P., Nijhof, A. M. and Jongejan, F. (2004). Confirmation of occurrence of Babesia canis vogeli in domestic dogs in South Africa. Veterinary Parasitology 122, 119-125. (Pubitemid 38737305)
35. Nei, M. and Kumar, S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press, New York, USA.
36. Neitz, W. O. (1957). Theileriosis, gonderiosis and cytauxzoonoses: a review. Onderstepoort Journal of Veterinary Research 27, 275-430.
37. Neitz, W. O., Canham, A. S. and Kluge, E. (1955). Corridor disease: A fatal form of bovine theileriosis encountered in Zululand. Journal of the South African Veterinary Association 26, 79-87.
38. Nijhof, A. M., Penzhorn, B. L., Lynen, G., Mollel, J. O., Morkel, P., Bekker, C. P. 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. (Pubitemid 36576580)
39. Nijhof, A. M., Pillay, V., Steyl, J., Prozesky, L., Stoltsz, W. H., Lawrence, J. A., Penzhorn, B. L. 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. (Pubitemid 43100636)
40. Norval, R. A., Lawrence, J. A., Young, A. S., Perry, B. D., Dolan, T. T. and Scott, J. (1991). Theileria parva: influence of vector, parasite and host relationships on the epidemiology of theileriosis in southern Africa. Parasitology 102, 347-356.
41. Norval, R. A. I., Perry, B. D., Young, A. S. (1992). The Epidemiology of Theileriosis in Africa. Academic Press, London, UK.
42. Oosthuizen, M. C., Zweygarth, E., Collins, N. E., Troskie, M. and Penzhorn, B. L. (2008). Identification of a novel Babesia sp. from a sable antelope (Hippotragus niger Harris, 1838). Journal of Clinical Microbiology 46, 2247-2251.
43. Pain, A., Renauld, H., Berriman, M., Murphy, L., Yeats, C. A., Weir, W., Kerhornou, A., Aslett, M., Bishop, R., Bouchier, C., Cochet, M., Coulson, R. M., Cronin, A., de Villiers, E. P., Fraser, A., Fosker, N., Gardner, M., Goble, A., Griffiths-Jones, S., Harris, D. E., Katzer, F., Larke, N., Lord, A., Maser, P., McKellar, S., Mooney, P., Morton, F., Nene, V., O'Neil, S., Price, C., Quail, M. A., Rabbinowitsch, E., Rawlings, N. D., Rutter, S., Saunders, D., Seeger, K., Shah, T., Squares, R., Squares, S., Tivey, A., Walker, A. R., Woodward, J., Dobbelaere, D. A., Langsley, G., Rajandream, M. A., McKeever, D., Shiels, B., Tait, A., Barrell, B. and Hall, N. 2005). Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 309 131-133. (Pubitemid 40934991)
44. Potgieter, F. T., Stoltsz, W. H., Blouin, E. F. and Roos, J. A. (1988). Corridor disease in South Africa: a review of the current status. Journal of the South African Veterinary Association 59, 155-160. (Pubitemid 18262486)
45. Reichard, M. V., Van Den Bussche, R. A., Meinkoth, J. H., Hoover, J. P. and Kocan, A. A. (2005). A new species of Cytauxzoon from Pallas' cats caught in Mongolia and comments on the systematics and taxonomy of piroplasmids. Journal of Parasitology 91, 420-426. (Pubitemid 40756282)
46. Sibeko, K. P., Geysen, D., Oosthuizen, M. C., Matthee, C. A., Troskie, M., Potgieter, F. T., Coetzer, J. A. and Collins, N. E. (2010). Four p67 alleles identified in South African Theileria parva field samples. Veterinary Parasitology 167, 244-254.
47. Sibeko, K. P., Oosthuizen, M. C., Collins, N. E., Geysen, D., Rambritch, N. E., Latif, A. A., Groeneveld, H. T., Potgieter, F. T. and Coetzer, J. A.(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.
48. Simmons, M. P., Zhang, L. B., Webb, C. T. and Reeves, A. (2006). How can third codon positions outperform first and second codon positions in phylogenetic inference? An empirical example from the seed plants. Systematic Biology 55, 245-258.
49. Stagg, D. A., Young, A. S., Leitch, B. L., Grootenhuis, J. G. and Dolan, T. T. (1983). Infection of mammalian cells with Theileria species. Parasitology 86, 243-254.
50. Stewart, N. P., De Vos, A. J., Shiels, I. and McGregor, W. (1987). The experimental transmission of Theileria buffeli of cattle in Australia by Haemaphysalis humerosa. Australian Veterinary Journal 64, 81-83.
51. Stewart, N. P., Uilenberg, G. and De Vos, A. J. (1996). Review of Australian species of Theileria, with special reference to Theileria buffeli of cattle. Tropical Animal Health Production 28, 81-90. (Pubitemid 126725607)
52. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596-1599. (Pubitemid 47236692)
53. Theiler, A. (1904). Rhodesian tick fever. Transvaal Agricultural Journal 2, 421-438.
54. Theiler, A. (1906). Piroplasma mutans (n. spec) of South African cattle. The Journal of Comparative Pathology and Therapeutics 19, 292-300.
55. Tonetti, N., Berggoetz, M., Rühle, C., Pretorius, A. M. and Gern, L. (2009). Ticks and tick-borne pathogens from wildlife in the Free State Province, South Africa. Journal of Wildlife Diseases 45, 437-446.
56. Uilenberg, G. (1964). Haemotoxenus veliferus, n. g., n. sp., parasite incertae sedis du sang de bovins a Madagascar. Revue d'élevage et de médecine vétérinaire des pays tropicaux 17, 655-662.
57. Uilenberg, G. (1976). Tick-borne livestock diseases and their vectors. 2. Epizootiology of tick-borne diseases. World Animal Review 17, 8-15.
58. Uilenberg, G. (1981). Theilerial species of domestic livestocks. In Advances in the Control of Theileriosis (ed. Irvin, A. D., Cunningham, M. P. and Young, A. S.), pp. 4-37. Martinus Nijhoff Publishers, The Hague, The Netherlands.
59. Uilenberg, G. (2006). Babesia -A historical perspective. Veterinary Parasitology 138, 3-10.
60. Uilenberg, G. and Schreuder, B. E. (1976). Studies on Theileriidae (Sporozoa) in Tanzania. I. Tick transmission of Haematoxenus veliferus. Tropenmedizin und Parasitologie 27, 106-111.
61. Young, A. S. (1981). The epidemiology of theileriosis in East Africa. In Advances in the Control of Theileriosis (ed. Irvin, A. D., Cunningham, M. P. and Young, A. S.), pp. 38-55. Martinus Nijhoff Publishers, The Hague, The Netherlands.
62. Young, A. S., Brown, C. G., Burridge, M. J., Grootenhuis, J. G., Kanhai, G. K., Purnell, R. E. and Stagg, D. A. (1978a). The incidence of theilerial parasites in East African buffalo (Syncerus caffer). Tropenmedizin und Parasitologie 29, 281-288. (Pubitemid 9020200)
63. Young, A. S., Grootenhuis, J. G., Kimber, C. D., Kanhai, G. K. and Stagg, D. A. (1977). Isolation of a Theileria species from Eland (Taurotragus oryx) infective for cattle. Tropenmedizin und Parasitologie 27, 185-194. (Pubitemid 8117760)
64. Young, A. S., Purnell, R. E., Payne, R. C., Brown, C. G. and Kanhai, G. K. (1978b). Studies on the transmission and course of infection of a Kenyan strain of Theileria mutans. Parasitology 76, 99-115.
65. Zweygarth, E., Koekemoer, O., Josemans, A. I., Rambritch, N., Pienaar, R., Putterill, J., Latif, A. and Potgieter, F. T. (2009). Theileriainfected cell line from an African buffalo (Syncerus caffer). Parasitology Research 105, 579-581.