Theileria lestoquardi in Sudan is highly diverse and genetically distinct from that in Oman

Awad, Hoyam; Al-Hamidhi, Salama; Hussein, Abdel Rahim M. El; Yousif, Younis Mohammed zein; Taha, Khalid M.; Salih, Diaeldin A.; Weir, William; Babiker, Hamza A.

doi:10.1016/j.meegid.2018.04.014

Cited by 8 publications

(12 citation statements)

References 36 publications

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“…Almost all infected animals displayed a novel (or combination of) genotype (defined by unique combinations of alleles detected by the examined microsatellites), including strains extracted from dead animals. This is consistent with the high genetic diversity and multiplicity of infection reported for T. lestoquardi populations in Oman 7 and Sudan 25 . Moreover, the observed increase in T. lestoquardi multiplicity of infection over time can be attributed to super-infection and the consecutive acquisition of novel genotypes combined with delayed clearance of initial infecting parasites.…”

Section: Discussionsupporting

confidence: 89%

Dynamics and within-host interaction of Theileria lestoquardi and T. ovis among naive sheep in Oman

Awad

Gadalla

Postigo

et al. 2020

Sci Rep

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Mixed species infections of Theileria spp. are common in nature. Experimental and epidemiological data suggest that mixed species infections elicit cross-immunity that can modulate pathogenicity and disease burden at the population level. The present study examined within-host interactions, over a period of 13 months during natural infections with two Theileria spp., pathogenic (T. lestoquardi) and non-pathogenic (T. ovis), amongst a cohort of naive sheep in Oman. In the first two months after exposure to infection, a high rate of mortality was seen among sheep infected with T. lestoquardi alone. However, subsequently mixed-infections of T. lestoquardi and T. ovis prevailed, and no further death occurred. The overall densities of both parasite species were significantly higher as single infection vs mixed infection and the higher relative density of pathogenic T. lestoquardi indicated a competitive advantage over T. ovis in mixed infection. The density of both species fluctuated significantly over time, with no difference in density between the very hot (May to August) and warm season (September to April). A high degree of genotype multiplicity was seen among T. lestoquardi infections, which increased with rising parasite density. Our results illustrate a potential competitive interaction between the two ovine Theileria spp., and a substantial reduction in the risk of mortality in mixed parasite infections, indicating that T. ovis confers heterologous protection against lethal T. lestoquardi infection.

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Section: Discussionsupporting

confidence: 89%

Dynamics and within-host interaction of Theileria lestoquardi and T. ovis among naive sheep in Oman

Awad

Gadalla

Postigo

et al. 2020

Sci Rep

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“…This can be attributed to high abundance and infestation of Hyalomma anatolicum, which can promote cross-mating and recombination within ticks to generate novel parasite genotypes for infection of sheep. The above is consistent with the high genetic diversity and multiplicity of infection reported for T. lestoquardi populations in Oman [6] and Sudan [24].…”

Section: Discussionsupporting

confidence: 90%

“…This moderate level of differentiation is consistent with the data from similar analysis between T. annulata in Tunisia and Turkey (F ST values of 0.049) [25]. A more profound genetic differentiation has been observed between T. annulata and T. lestoquardi in Oman and populations in widely separated countries, consistent with geographical and trade barriers hindering gene ow [6,18,24]. For example, a high level of differentiation (F ST = 0.295) was evident between T. lestoquardi populations in Oman and Sudan, while no temporal differentiation was observed between T. lestoquardi population collected in Sudan in 2013 compared to 2016 (F ST = 0.29) [24].…”

Section: Discussionsupporting

confidence: 86%

A Comparative Study of Single Theileria Lestoquardi and Mixed Infections with Theileria Ovis

Al-Hamidhi

Elshafie

Morrison

et al. 2021

Preprint

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Background: Epidemiological surveys in Oman have revealed a high prevalence of the co-occurrence of the pathogenic T. lestoquardi and the non-pathogenic T. ovis among sheep in the Barka region, Oman. Our most recent data illustrated an interaction and reduced mortality risk in animals co-infected with T. lestoquardi and T. ovis, suggesting that the latter confers protection against pathogenicity of T. lestoquardi. The present study extends the above findings and examines disease outcomes; clinical markers, hematological parameters and parasite density in mixed and single T. lestoquardi infections. Methods: A total of 390 blood samples were collected from 16 sheep pens located in Barka, Oman between July and November 2019. Theileria spp were detected and quantified using qPCR assay targeting 18S rRNA, and the extent of genetic diversity was estimated by a panel of T. lestoquardi specific micro- and mini-satellites. The association of some disease markers with the presence of Theileria spp. and genetic diversity was tested. Results: Theileria spp were detected in 75 (19.2%) sheep; of these 65 (86.7%) had mixed infections (T. lestoquardi plus T. ovis), 8 (10.6%) were infected with T. lestoquardi alone and 2 (2.7%) with only T. ovis. Exotic breeds had a higher risk for Theileria spp infection. The density of both parasites was higher in single infection against mixed infection, and there was a relatively lower density of T. lestoquardi in mixed infections. However, there was no difference in hematological indices between single T. lestoquardi and mixed infections. High genetic diversity was observed among T. lestoquardi in Barka, with no differences of T. lestoquardi in single and mixed infections. The extent of diversity seen in Barka was higher (He = 0.772) than that reported in Oman in 2019 (He = 0.582), with distinct T. lestoquardi genotypes. Conclusion: The substantial prevalence of T. lestoquardi as mixed vs single infection supports the hypothesis that T. ovis confers protection against lethal T. lestoquardi infection. However, there were no differences in disease correlations (clinical markers, hematology parameters and density of parasites) or the extent of diversity of T. lestoquardi between the two types of infection. The presence of distinct T. lestoquardi genotypes in Barka, compared to that reported earlier in Oman, highlights the need for further analysis of the parasite populations to inform on novel approaches for controlling malignant theileriosis.

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“…As measured using expected heterozygosity, the overall genetic diversity of the B. ovis population in Turkey was found to be extremely high (H e = 0.799) and similar to that observed for its phylogenetically closest relative, the cattle-infecting B. bovis (H e =0.837) . Likewise, in a recent study comparing reference isolates from diverse countries and continents around the world, a comparably high genetic diversity was observed in the B. bovis metapopulation (H e = 0.780, Flores et al, 2013 (Simuunza et al, 2011;Al-Hamidhi et al, 2016;Ali et al, 2017;Awad et al, 2018). While each of these species was analysed using a different set of markers, these various markers were identified using broadly similar criteria and for this reason they are broadly comparable.…”

Section: Discussionmentioning

confidence: 99%

“…annulata is because present day T. lestoquardi and T. annulata evolved relatively recently from a common ancestor, following adaptation of T. lestoquardi to the small ruminant host, as supported by high 18S rRNA gene identity (Schnittger et al, 2000(Schnittger et al, , 2003Awad et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

High genetic diversity and differentiation of theBabesia ovispopulation in Turkey

Mira

Ünlü

Bilgiç

et al. 2019

Transbound Emerg Dis

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Babesia ovis is a tick-transmitted protozoan hemoparasite causing ovine babesiosis in sheep and goats leading to considerable economic loss in Turkey and neighboring countries. There are no vaccines available, therapeutic drugs leave toxic residues in meat and milk, and tick vector control entails environmental risks. A panel of eight mini-and microsatellite marker loci was developed and applied to study genetic diversity and substructuring of B. ovis from western, central, and eastern Turkey. A high genetic diversity (H e = 0.799) was found for the sample of the overall B. ovis population (n = 107) analyzed. Principle component analysis (PCoA) revealed the existence of three parasite subpopulations: (i) a small subpopulation of isolates from Aydin, western Turkey, (ii) a second cluster predominantly generated by isolates from western Turkey, and (iii) a third cluster predominantly formed by isolates from central and eastern Turkey. Two B. ovis isolates from Israel included in the analysis clustered with isolates from central and eastern Turkey. This finding strongly suggests substructuring of a major Turkish population into western vs. central-eastern subpopulations, while the additional smaller B. ovis population found in Aydin could have been introduced, more recently, to Turkey. STRUCTURE analysis suggests a limited exchange of parasite strains between the western and the central-eastern regions and vice versa, possibly due to limited trading of sheep. Importantly, evidence for recombinant genotypes was obtained in regionally interchanged parasite isolates. Important climatic differences between the western and the central/eastern region, with average yearly temperatures of 21ºC versus 15ºC, correspond with the identified geographical substructuring. We hypothesize that the different climatic conditions may result in variation in the activity of subpopulations of Rhipicephalus spp. tick vectors, which, in turn, could selectively maintain and transmit different parasite populations. These findings may have important implications for vaccine development and the spread of drug resistance.

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Theileria lestoquardi in Sudan is highly diverse and genetically distinct from that in Oman

Cited by 8 publications

References 36 publications

Dynamics and within-host interaction of Theileria lestoquardi and T. ovis among naive sheep in Oman

Dynamics and within-host interaction of Theileria lestoquardi and T. ovis among naive sheep in Oman

A Comparative Study of Single Theileria Lestoquardi and Mixed Infections with Theileria Ovis

High genetic diversity and differentiation of theBabesia ovispopulation in Turkey

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