Divergence of the Mitochondrial Genome Structure in the Apicomplexan Parasites, Babesia and Theileria

Abstract

Mitochondrial (mt) genomes from diverse phylogenetic groups vary considerably in size, structure, and organization. The genus Plasmodium, causative agent of malaria, of the phylum Apicomplexa, has the smallest mt genome in the form of a circular and/or tandemly repeated linear element of 6 kb, encoding only three protein genes (cox1, cox3, and cob). The closely related genera Babesia and Theileria also have small mt genomes (6.6 kb) that are monomeric linear with an organization distinct from Plasmodium. To elucidate the structural divergence and evolution of mt genomes between Babesia/Theileria and Plasmodium, we determined five new sequences from Babesia bigemina, B. caballi, B. gibsoni, Theileria orientalis, and T. equi. Together with previously reported sequences of B. bovis, T. annulata, and T. parva, all eight Babesia and Theileria mt genomes are linear molecules with terminal inverted repeats (TIRs) on both ends containing three protein-coding genes (cox1, cox3, and cob) and six large subunit (LSU) ribosomal RNA (rRNA) gene fragments. The organization and transcriptional direction of protein-coding genes and the rRNA gene fragments were completely conserved in the four Babesia species. In contrast, notable variation occurred in the four Theileria species. Although the genome structures of T. annulata and T. parva were nearly identical to those of Babesia, an inversion in the 3-kb central region was found in T. orientalis. Moreover, the T. equi mt genome is the largest (8.2 kb) and most divergent with unusually long TIR sequences, in which cox3 and two LSU rRNA gene fragments are located. The T. equi mt genome showed little synteny to the other species. These results suggest that the Theileria mt genome is highly diverse with lineage-specific evolution in two Theileria species: genome inversion in T. orientalis and gene-embedded long TIR in T. equi.

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

“…Unlike their plastid counterparts, dinoflagellate mtDNAs can contain noncanonical start and stop codons (or none at all), transspliced genes, and oligonucleotide caps at both the 5′ and 3′ ends of transcripts (36,68). Many of these tendencies are consistent across other major alveolate groups as well (47,56,63,73).…”

“…At one extreme are the giant mtDNAs of seed plants, like cucumber (∼1.6 Mb) (49) and Silene conica (∼11 Mb) (40), as well as those of diplonemids, which can exceed 500 kb (51). At the other end of the spectrum are the 6-kb mtDNAs of certain apicomplexans (56) and the fragmented mtDNA of their close relative C. velia, which is even smaller (57). Diminutive mtDNAs (<13 kb) have also been uncovered in green algae (44), ctenophores (58), and fungi (59).…”

“…As with size and structure, mtDNAs show greater variation in gene number and organization than ptDNAs (12). The jakobid Andalucia godoyi has the largest, least-derived mitochondrial gene content (100 genes, ∼66 of which encode proteins) (67), whereas dinoflagellates, apicomplexans, and their close relatives have the most reduced: three or fewer proteins, no tRNAs, and in some instances (e.g., C. velia) even lack complete rRNAs (36,56,57,68). Chlamydomonadalean mtDNAs also have diminished coding contents (10-13 genes) (44), and some land plants (e.g., S. moellendorffii), animals (e.g., the winged box jellyfish), and trypanosomes have lost all or most of their mitochondrial tRNA-coding regions (39,42,48).…”

Involvement of Mitochondrial Genes of <i>Babesia gibsoni</i> in Resistance to Diminazene Aceturate

“…The lengths of mtDNa from B. gibsoni in our laboratory were 5,867 base pairs. The mtDNa of the B. gibsoni consisted of three functional genes, COXI, COXIII, and CYTb, and six discontinuous ribosomal RNA, as Hikosaka et al previously reported (NrcPD strain) [7]. additionally, terminal inverted …”

“…These results indicated that Da did not directly affect mtDNa of the Da-resistant B. gibsoni. in general, COXI is one of 13 subunits of cytochrome c oxidase (complex iV), which is essential for electron transfer as a terminal oxidase in the respiratory chain [7,28]. COXIII is highly conserved in most of the heme-copper respiratory oxidase superfamily and is considered to be involved in the assembly and stabilization of the entire complex [7,28].…”