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South African Buffalo-Derived Theileria Parva Is Distinct from Other Buffalo and Cattle-Derived T fgene-12-666096 June 25, 2021 Time: 18:23 # 1 ORIGINAL RESEARCH published: 25 June 2021 doi: 10.3389/fgene.2021.666096 South African Buffalo-Derived Theileria parva Is Distinct From Other Buffalo and Cattle-Derived T. parva Boitumelo B. Maboko1,2*, Kgomotso P. Sibeko-Matjila2, Rian Pierneef3, Wai Y. Chan3, Antoinette Josemans1, Ratselane D. Marumo1, Sikhumbuzo Mbizeni1,4, Abdalla A. Latif5 and Ben J. Mans1,2,6* 1 Agricultural Research Council, Onderstepoort Veterinary Research, Pretoria, South Africa, 2 Department of Veterinary Tropical Diseases, University of Pretoria, Pretoria, South Africa, 3 Agricultural Research Council, Biotechnology Platform, Pretoria, South Africa, 4 Department of Agriculture and Animal Health, University of South Africa, Pretoria, South Africa, 5 School of Life Sciences, University of KwaZulu Natal, Durban, South Africa, 6 Department of Life and Consumer Sciences, University of South Africa, Pretoria, South Africa Theileria parva is a protozoan parasite transmitted by the brown-eared ticks, Edited by: Rhipicephalus appendiculatus and Rhipicephalus zambeziensis. Buffaloes are the Jun-Hu Chen, National Institute of Parasitic parasite’s ancestral host, with cattle being the most recent host. The parasite has two Diseases, China transmission modes namely, cattle–cattle and buffalo–cattle transmission. Cattle–cattle Reviewed by: T. parva transmission causes East Coast fever (ECF) and January disease syndromes. Isaiah Obara, Buffalo to cattle transmission causes Corridor disease. Knowledge on the genetic Freie Universität Berlin, Germany Erik Bongcam-Rudloff, diversity of South African T. parva populations will assist in determining its origin, Swedish University of Agricultural evolution and identify any cattle–cattle transmitted strains. To achieve this, genomic Sciences, Sweden DNA of blood and in vitro culture material infected with South African isolates (8160, *Correspondence: Boitumelo B. Maboko 8301, 8200, 9620, 9656, 9679, Johnston, KNP2, HL3, KNP102, 9574, and 9581) were [email protected] extracted and paired-end whole genome sequencing using Illumina HiSeq 2500 was Ben J. Mans performed. East and southern African sample data (Chitongo Z2, Katete B2, Kiambu [email protected] Z464/C12, Mandali Z22H10, Entebbe, Nyakizu, Katumba, Buffalo LAWR, and Buffalo Specialty section: Z5E5) was also added for comparative purposes. Data was analyzed using BWA This article was submitted to and SAMtools variant calling with the T. parva Muguga genome sequence used as a Evolutionary and Genomic Microbiology, reference. Buffalo-derived strains had higher genetic diversity, with twice the number a section of the journal of variants compared to cattle-derived strains, confirming that buffaloes are ancestral Frontiers in Genetics reservoir hosts of T. parva. Host specific SNPs, however, could not be identified among Received: 09 February 2021 Accepted: 27 May 2021 the selected 74 gene sequences. Phylogenetically, strains tended to cluster by host Published: 25 June 2021 with South African buffalo-derived strains clustering with buffalo-derived strains. Among Citation: the buffalo-derived strains, South African strains were genetically divergent from other Maboko BB, Sibeko-Matjila KP, buffalo-derived strains indicating possible geographic sub-structuring. Geographic sub- Pierneef R, Chan WY, Josemans A, Marumo RD, Mbizeni S, Latif AA and structuring was also observed within South Africa strains. The knowledge generated Mans BJ (2021) South African from this study indicates that to date, ECF is not circulating in buffalo from South Africa. It Buffalo-Derived Theileria parva Is Distinct From Other Buffalo also shows that T. parva has historically been present in buffalo from South Africa before and Cattle-Derived T. parva. the introduction of ECF and was not introduced into buffalo during the ECF epidemic. Front. Genet. 12:666096. doi: 10.3389/fgene.2021.666096 Keywords: Theileria parva, whole genome sequencing, cattle, buffalo, genetic diversity, South Africa Frontiers in Genetics| www.frontiersin.org 1 June 2021| Volume 12| Article 666096 fgene-12-666096 June 25, 2021 Time: 18:23 # 2 Maboko et al. South African Buffalo-Derived Theileria parva INTRODUCTION (Yusufmia et al., 2010) as well as strains with antigenic gene sequences identical to the Muguga isolate (Sibeko et al., 2010, Theileria parva is a protozoan parasite transmitted by brown- 2011) have been reported in KwaZulu-Natal, raising concerns eared ticks, Rhipicephalus appendiculatus and Rhipicephalus of the possible circulation of ECF strains in South Africa. zambeziensis (Blouin and Stoltsz, 1989). Cape buffaloes are The animals, however, lost their parasite load approximately considered the parasite’s ancestral host, with cattle being a 120 days post infection and could not transmit the parasite more recent host (Norval et al., 1991). The parasite has (Mbizeni et al., 2013). two transmission modes namely, cattle–cattle and buffalo– There is genetic evidence that phenotypic differences between cattle transmission. Cattle–cattle T. parva transmission by ticks cattle-derived and buffalo-derived parasite strains have an causes East Coast fever (ECF) and January disease syndromes underlying genetic component. A deletion in the p67 gene (Theiler, 1904; Lawrence, 1979). East Coast fever is endemic in (allele 1) has been associated with strains of cattle origin, different East and southern African countries, notably Kenya, whereas lack of that deletion indicated buffalo origin (allele Rwanda, Tanzania, Uganda, Malawi, Mozambique, and Zambia 2) (Nene et al., 1996). The observation that cattle-derived (Lawrence et al., 1992, 2017). The name East Coast fever T. parva showed genotypes found in buffalo was first observed is derived from the historical origin of the disease in the in South Africa (Sibeko et al., 2010) later confirmed by East Coast of Africa (Theiler, 1904). South Africa had ECF Mukolwe et al.(2020) and Mwamuye et al.(2020) using outbreaks in the early 1900s that caused extensive mortalities strains from various countries. Sibeko et al.(2010) found before its eradication in the country in the 1950s (Potgieter both alleles and additional ones in South African strains, et al., 1988; Norval et al., 1992). January disease is only irrespective of host origin indicating that South African reported in Zimbabwe (Lawrence, 1992; Geysen et al., 1999). populations are different from East African populations. Thus, These diseases cause major cattle and financial losses with the p67 gene could not differentiate host-derived T. parva in January disease’s seasonality making it the milder of the two South Africa. On the other hand, 200 random genes selected by diseases due to lesser mortalities (Matson, 1967; Lawrence, 1979; Hayashida et al.(2013) showed phylogenetic differentiation of the Norval et al., 1992). different host strains. Buffalo–cattle transmission causes a disease known as Characterization of T. parva has been extensively done using Corridor disease. The name is derived from an outbreak reported various loci specific molecular tools. Bishop et al.(2001) used between the corridor of the then Hluhluwe and Imfolozi PIM and p104 to identify different cattle-derived T. parva nature reserves (Neitz et al., 1955). Currently, Corridor disease isolates, which was supported by Norling et al.(2015) using is endemic in certain regions of South Africa, Mpumalanga, whole genome sequencing. In addition, Pelle et al.(2011) Limpopo, and KwaZulu-Natal provinces where cattle and game found that a less diverse population subset of T. parva is share grazing land (Potgieter et al., 1988; Stoltsz, 1989; Mbizeni maintained in cattle for cattle–cattle transmission. Microsatellites et al., 2013). It is very lethal to cattle to an extent that parasites have found buffalo-derived strains to be geographically diverse rarely reach the tick-infective piroplasm stage in this host. If and the strains to be distinct from cattle-derived strains. piroplasms are present, they are not regularly transmitted to They have also shown evidence of allele sharing among hosts cattle (Young et al., 1973; Uilenberg, 1999; Morrison, 2015). in different countries (Oura et al., 2011; Elisa et al., 2014; Barnett and Brocklesby(1966) showed that passage of buffalo- Hemmink et al., 2018). derived T. parva in cattle transforms the parasite to become Next generation sequencing (NGS) has opened various cattle–cattle transmitted T. parva (Lawrence, 1992). Conversely, avenues for research into genomic diversity. In T. parva Potgieter et al.(1988) could not reproduce the transformation for example, NGS allowed access to additional markers to of South African buffalo-derived T. parva to resemble ECF characterize the parasite and discriminate ECF and Corridor strains. The latter study suggested that possible selection of disease on a genome-wide scale (Gardner et al., 2005; Hayashida cattle infective strains instead of behavioral change of the et al., 2013; Norling et al., 2015). In spite of the distinction parasite may have been responsible for what was reported as between cattle-derived and buffalo-derived strains, regions “transformation.” responsible for this are yet to be identified. It is thus important Recovery from T. parva infection can result in cattle being to identify genetic loci linked to buffalo-transmitted T. parva immune to specific parasite strains, but remain piroplasm carriers (Corridor disease) only and not cattle–cattle transmitted T. parva that are able to transmit the parasite to other susceptible (January disease
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