Comparative genomics reveals unique features of two Babesia motasi subspecies: Babesia motasi lintanensis and Babesia motasi hebeiensis

Babesiosis is caused by species of the genus Babesia that are mainly transmitted by ticks, and less commonly through blood product transfusion and transplacentally (Lantos and Krause, 2002, Ord and Lobo, 2015). The organisms of this genus were first described by Babes in 1888 when he investigated bovine hemoglobinuria in Romania. Currently, more than 100 Babesia spp. have been identified worldwide and they impose a significant burden on domestic animals (Vannier et al., 2015). During the past 50 years, increasing numbers of Babesia spp. have been identified as a cause of human infection throughout the world, including Babesia microti, Babesia divergens, Babesia duncani, Babesia crassa, and Babesia motasi (Conrad et al., 2006, Gray et al., 2010, Bloch et al., 2012, Cornillot et al., 2012). As an infectious agent affecting humans and small ruminants, B. motasi has a wide distribution (Africa, Asia, and Europe); cases of B. motasi infective to humans were reported in 2005 and 2019 (Conrad et al., 2006, Kim et al., 2007, Jia et al., 2018, Hong et al., 2019).

Babesia motasi, a large species of Babesia sensu stricto, is transmitted by Haemaphysalis spp. ticks and invades erythrocytes of vertebrate hosts (Jalovecka et al., 2019). The clinical signs of infected animals vary on the basis of the parasite strains and animal breeds. Some strains are not pathogenic to intact sheep, whereas infections of splenectomised animals caused weight loss, fever, anorexia, lassitude and anemia. However, some of strains have high pathogenicity (Uilenberg et al., 1980, Lewis et al., 1981, Guan et al., 2010). The infected intact or splenectomised sheep and goats show lack of appetite, weight loss, fever, serious anemia, haemoglobinuria and even death. In fact, variable clinical sings of infected animals might partially result from B. motasi strains or subspecies, and infections may consist of at least two species or subspecies, distinct in pathogenicity, serology, and morphology (Uilenberg et al., 1980, Lewis et al., 1981, Yin et al., 1997, Bai et al., 2002, Uilenberg, 2006). A low pathogenicity B. motasi species/subspecies was originally discovered in northern Europe, while a high pathogenicity B. motasi was described in southern Europe and the Mediterranean basin (Uilenberg et al., 1980, Lewis et al., 1981). In China, four B. motasi strains, B. motasi Lintan, B. motasi Tianzhu, B. motasi Hebei, and B. motasi Ningxian, were isolated from sheep by the Vector and Vector-Borne Diseases (VVBD) Laboratory, Lanzhou Veterinary Research Institute (LVRI), China, between 1992–2012 (Bai et al., 2002, Liu et al., 2007). These strains could be separated into two subspecies (B. motasi Lintan and B. motasi Hebei) based on their distinct characteristics in morphology, serology, pathogenicity, cultural features, and virulence. Additionally, this proposal was supported by phylogenetic analysis targeting the 18S rRNA gene, internal transcribed spacer sequence (ITS), and heat shock protein 90 (HSP90) gene (Bai et al., 2002, Niu et al., 2009, Tian et al., 2013a, 2013b). Recently, comparative analysis of apicoplast genomes and mitochondrial genomes of the four Chinese B. motasi strains placed the isolates in two separate clades: B. motasi Lintan and B. motasi Tianzhu in the same clade, and B. motasi Hebei and B. motasi Ningxian in another clade (Wang et al., 2019b, 2020). In the following text, we refer to B. motasi Lintan as Babesia motasi lintanensis and B. motasi Hebei as Babesia motasi hebeiensis. Until now, all comparisons between these two subspecies have been performed primarily on amplified fragments of the nuclear genome or genes of parasite organelles (apicoplast and mitochondrion).

As an emerging and reemerging cause of human babesiosis, and with the observation of severe and even fatal human cases associated with B. motasi, it is worthwhile to explore the biological features, adaptive evolution, and the host–parasite interaction driving the generation of whole genomes of pathogens. In this context, we selected B. m. lintanensis and B. m. hebeiensis as representative strains of each species to perform genome sequencing. We performed comparative genomic analysis to reveal critical features about genome organization and provide new insights into B. motasi biology, as follows: i) exploring regulators responsible for differential gene expression, such as transcription factors; ii) identifying molecules/components relating to host cell invasion and gliding motility, including glideosome, moving junction (MJ), spherical body proteins (SBPs), rhoptry associated proteins (RAPs), and Trombospondin-related anonymous protein (TRAP); and iii) confirming phylogenetic relationships of B. m. lintanensis and B. m. hebeiensis with other apicomplexan parasites, and revealing significant features of these genomes (e.g., high repeat sequence, species-specific gene families and long terminal repeat retrotransposons).

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