Piroplasms in Brown Hyaenas (Parahyaena Brunnea) and Spotted Hyaenas (Crocuta Crocuta) in Namibia and South Africa Are Closely Related to Babesia Lengau

Overview

Journal Parasitol Res

Specialty Parasitology

Date 2016 Dec 4

PMID 27913878

Citations 4

Authors

Richard E J Burroughs

Barend L Penzhorn

Ingrid Wiesel

Nancy Barker

Ilse Vorster

Marinda C Oosthuizen

Affiliations

Soon will be listed here.

Abstract

The objective of our study was identification and molecular characterization of piroplasms and rickettsias occurring in brown (Parahyaena brunnea) and spotted hyaenas (Crocuta crocuta) from various localities in Namibia and South Africa. Whole blood (n = 59) and skin (n = 3) specimens from brown (n = 15) and spotted hyaenas (n = 47) were screened for the presence of Babesia, Theileria, Ehrlichia and Anaplasma species using the reverse line blot (RLB) hybridization technique. PCR products of 52/62 (83.9%) of the specimens hybridized only with the Theileria/Babesia genus-specific probes and not with any of the species-specific probes, suggesting the presence of a novel species or variant of a species. No Ehrlichia and/or Anaplasma species DNA could be detected. A parasite 18S ribosomal RNA gene of brown (n = 3) and spotted hyaena (n = 6) specimens was subsequently amplified and cloned, and the recombinants were sequenced. Homologous sequence searches of databases indicated that the obtained sequences were most closely related to Babesia lengau, originally described from cheetahs (Acinonyx jubatus). Observed sequence similarities were subsequently confirmed by phylogenetic analyses which showed that the obtained hyaena sequences formed a monophyletic group with B. lengau, B abesia conradae and sequences previously isolated from humans and wildlife in the western USA. Within the B. lengau clade, the obtained sequences and the published B. lengau sequences were grouped into six distinct groups, of which groups I to V represented novel B. lengau genotypes and/or gene variants. We suggest that these genotypes cannot be classified as new Babesia species, but rather as variants of B. lengau. This is the first report of occurrence of piroplasms in brown hyaenas.

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References

Staden R, Beal K, Bonfield J . The Staden package, 1998. Methods Mol Biol. 1999; 132:115-30. DOI: 10.1385/1-59259-192-2:115. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Nijhof A, Penzhorn B, Lynen G, Mollel J, Morkel P, Bekker C . Babesia bicornis sp. nov. and Theileria bicornis sp. nov.: tick-borne parasites associated with mortality in the black rhinoceros (Diceros bicornis). J Clin Microbiol. 2003; 41(5):2249-54. PMC: 154668. DOI: 10.1128/JCM.41.5.2249-2254.2003. View

Horak I, Braack L, Fourie L, Walker J . Parasites of domestic and wild animals in South Africa. XXXVIII. Ixodid ticks collected from 23 wild carnivore species. Onderstepoort J Vet Res. 2001; 67(4):239-50. View

Schnittger L, Rodriguez A, Florin-Christensen M, Morrison D . Babesia: a world emerging. Infect Genet Evol. 2012; 12(8):1788-809. DOI: 10.1016/j.meegid.2012.07.004. View

Nagore D, Garcia-Sanmartin J, Garcia-Perez A, Juste R, Hurtado A . Detection and identification of equine Theileria and Babesia species by reverse line blotting: epidemiological survey and phylogenetic analysis. Vet Parasitol. 2004; 123(1-2):41-54. DOI: 10.1016/j.vetpar.2004.04.010. View

Felsenstein J . CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP. Evolution. 2017; 39(4):783-791. DOI: 10.1111/j.1558-5646.1985.tb00420.x. View

Penzhorn B . Babesiosis of wild carnivores and ungulates. Vet Parasitol. 2006; 138(1-2):11-21. DOI: 10.1016/j.vetpar.2006.01.036. View

Kjemtrup A, Conrad P . A review of the small canine piroplasms from California: Babesia conradae in the literature. Vet Parasitol. 2006; 138(1-2):112-7. DOI: 10.1016/j.vetpar.2006.01.045. View

10.

Conrad P, Kjemtrup A, Carreno R, Thomford J, Wainwright K, Eberhard M . Description of Babesia duncani n.sp. (Apicomplexa: Babesiidae) from humans and its differentiation from other piroplasms. Int J Parasitol. 2006; 36(7):779-89. DOI: 10.1016/j.ijpara.2006.03.008. View

11.

Bosman A, Venter E, Penzhorn B . Occurrence of Babesia felis and Babesia leo in various wild felid species and domestic cats in Southern Africa, based on reverse line blot analysis. Vet Parasitol. 2006; 144(1-2):33-8. DOI: 10.1016/j.vetpar.2006.09.025. View

12.

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

13.

Leclaire S, Menard S, Berry A . Molecular characterization of Babesia and Cytauxzoon species in wild South-African meerkats. Parasitology. 2014; 142(4):543-8. DOI: 10.1017/S0031182014001504. View

14.

Kjemtrup A, Thomford J, Robinson T, Conrad P . Phylogenetic relationships of human and wildlife piroplasm isolates in the western United States inferred from the 18S nuclear small subunit RNA gene. Parasitology. 2000; 120 ( Pt 5):487-93. DOI: 10.1017/s003118209900582x. View

15.

Collins N, Allsopp B . Theileria parva ribosomal internal transcribed spacer sequences exhibit extensive polymorphism and mosaic evolution: application to the characterization of parasites from cattle and buffalo. Parasitology. 1999; 118 ( Pt 6):541-51. DOI: 10.1017/s0031182099004321. View

16.

Bekker C, de Vos S, Taoufik A, Sparagano O, Jongejan F . Simultaneous detection of Anaplasma and Ehrlichia species in ruminants and detection of Ehrlichia ruminantium in Amblyomma variegatum ticks by reverse line blot hybridization. Vet Microbiol. 2002; 89(2-3):223-38. DOI: 10.1016/s0378-1135(02)00179-7. View

17.

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. PMC: 8210823. DOI: 10.1093/molbev/msw054. View

18.

Altschul S, Gish W, Miller W, Myers E, Lipman D . Basic local alignment search tool. J Mol Biol. 1990; 215(3):403-10. DOI: 10.1016/S0022-2836(05)80360-2. View

19.

Apanaskevich D, Horak I, Camicas J . Redescription of Haemaphysalis (Rhipistoma) elliptica (Koch, 1844), an old taxon of the Haemaphysalis (Rhipistoma) leachi group from East and southern Africa, and of Haemaphysalis (Rhipistoma) leachi (Audouin, 1826) (Ixodida, Ixodidae). Onderstepoort J Vet Res. 2007; 74(3):181-208. DOI: 10.4102/ojvr.v74i3.122. View

20.

Bosman A, Oosthuizen M, Venter E, Steyl J, Gous T, Penzhorn B . Babesia lengau associated with cerebral and haemolytic babesiosis in two domestic cats. Parasit Vectors. 2013; 6:128. PMC: 3652746. DOI: 10.1186/1756-3305-6-128. View