Abstract
The class Hematozoa encompasses several clinically important genera, including Plasmodium, whose members cause the major life-threating disease malaria. Hence, a good understanding of the interrelationships of organisms from this class and reliable means for distinguishing them are of much importance. This study reports comprehensive phylogenetic and comparative analyses on protein sequences on the genomes of 28 hematozoa species to understand their interrelationships. In addition to phylogenetic trees based on two large datasets of protein sequences, detailed comparative analyses were carried out on the genomes of hematozoa species to identify novel molecular synapomorphies consisting of conserved signature indels (CSIs) in protein sequences. These studies have identified 79 CSIs that are exclusively present in specific groups of Hematozoa/Plasmodium species, also supported by phylogenetic analysis, providing reliable means for the identification of these species groups and understanding their interrelationships. Of these CSIs, six CSIs are specifically shared by all hematozoa species, two CSIs serve to distinguish members of the order Piroplasmida, five CSIs are uniquely found in all Piroplasmida species except B. microti and two CSIs are specific for the genus Theileria. Additionally, we also describe 23 CSIs that are exclusively present in all genome-sequenced Plasmodium species and two, nine, ten and eight CSIs which are specific for members of the Plasmodium subgenera Haemamoeba, Laverania, Vinckeia and Plasmodium (excluding P. ovale and P. malariae), respectively. Additionally, our work has identified several CSIs that support species relationships which are not evident from phylogenetic analysis. Of these CSIs, one CSI supports the ancestral nature of the avian-Plasmodium species in comparison to the mammalian-infecting groups of Plasmodium species, four CSIs strongly support a specific relationship of species between the subgenera Plasmodium and Vinckeia and three CSIs each that reliably group P. malariae with members of the subgenus Plasmodium and P. ovale within the subgenus Vinckeia, respectively. These results provide a reliable framework for understanding the evolutionary relationships among the Plasmodium/Piroplasmida species. Further, in view of the exclusivity of the described molecular markers for the indicated groups of hematozoa species, particularly large numbers of unique characteristics that are specific for all Plasmodium species, they provide important molecular tools for biochemical/genetic studies and for developing novel diagnostics and therapeutics for these organisms.
Highlights
The genus Plasmodium is comprised of eukaryotic unicellular parasites that parasitize a large variety of vertebrates [1,2,3]
conserved signature indels (CSIs), six CSIs are shared by all hematozoa species, two CSIs serve to distinguish members of the order Piroplasmida, five CSIs are uniquely found in all Piroplasmida species except B. microti and two CSIs are specific for the genus Theileria
CSIs in the homologs from all sequenced Plasmodium species, the genetic changes leading to these CSIs have likely occurred in a common ancestor of the genus Plasmodium, providing important molecular characteristics distinguishing this group of organisms from all others. Another interesting CSI identified by our analysis found in a highly conserved region of the protein cysteine-tRNA ligase is uniquely shared by all mammalian-infecting Plasmodium species, but it is not found in the members of the subgenus “Haemamoeba” consisting of the two avian infecting species viz. P. gallinaceum and P. relictum (Figure 4B)
Summary
The genus Plasmodium is comprised of eukaryotic unicellular parasites that parasitize a large variety of vertebrates [1,2,3]. The Babesia and Theileria genera, which are closely related to Plasmodium, are of much interest and contain species that are clinically significant [4,5,6]. Theileria species are responsible for the disease theileriosis affecting domestic cattle causing significant economic losses within the farming industry [7]. The genera Babesia and Theileria form the majority of the named members within the order Piroplasmida [8,9,10] and this order along with the genus. In view of the enormous clinical significance and economic impact of the members of the class Hematozoa [12,13,14], it is of much importance to reliably understand the interrelationships of different parasitic organisms that are part of this class and develop reliable means for distinguishing them from each other
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