Jumbled genomes: missing Apicomplexan synteny

Abstract

Whole-genome comparisons provide insight into genome evolution by informing on gene repertoires, gene gains/losses, and genome organization. Most of our knowledge about eukaryotic genome evolution is derived from studies of multicellular model organisms. The eukaryotic phylum Apicomplexa contains obligate intracellular protist parasites responsible for a wide range of human and veterinary diseases (e.g., malaria, toxoplasmosis, and theileriosis). We have developed an in silico protein-encoding gene based pipeline to investigate synteny across 12 apicomplexan species from six genera. Genome rearrangement between lineages is extensive. Syntenic regions (conserved gene content and order) are rare between lineages and appear to be totally absent across the phylum, with no group of three genes found on the same chromosome and in the same order within 25 kb up- and downstream of any orthologous genes. Conserved synteny between major lineages is limited to small regions in Plasmodium and Theileria/Babesia species, and within these conserved regions, there are a number of proteins putatively targeted to organelles. The observed overall lack of synteny is surprising considering the divergence times and the apparent absence of transposable elements (TEs) within any of the species examined. TEs are ubiquitous in all other groups of eukaryotes studied to date and have been shown to be involved in genomic rearrangements. It appears that there are different criteria governing genome evolution within the Apicomplexa relative to other well-studied unicellular and multicellular eukaryotes.

FIG. 1.

Species relationships and genome characteristics. A cladogram of investigated species with genome sizes, numbers of annotated protein-encoding genes, and numbers of chromosomes. Numbered labels on the cladogram indicate the different levels examined for ortholog cluster distribution. For example, level 1 contains ortholog clusters with members in all Apicomplexa. Level 5 contains ortholog clusters specific to Plasmodium falciparum, P. knowlesi, and P. vivax and not detected in the other apicomplexan species.

FIG. 2.

Detected synteny across the Apicomplexa. The circle is a graphical representation of the annotated chromosomes and contigs in each genome. Each species’ genome is labeled with the genus species abbreviation. Scaffolds/Contigs that are not assigned to chromosomes but contain syntenic regions are shown in black. Tick marks represent 1 Mb. Lines that span the interior of the circle connect syntenic regions as detected by MCSCAN. “Twisted” spans represent inversions. Different colors represent different chromosomes within each species.

FIG. 3.

Synteny between Plasmodium species. Each circle represents synteny between two species. Ticks = 100 kb. (A) P. falciparum and P. knowlesi, (B) P. falciparum and P. berghei, (C) P. vivax and P. knowlesi, and (D) P. berghei and P. chabaudi. Chromosome numbers are indicated following the species abbreviation. Different colors represent different chromosomes within each species.

FIG. 4.

Synteny between Theileria and Babesia species. Each circle represents synteny between two species. Ticks = 100 kb. (A) T. annulata and T. parva and (B) T. annulata and B. bovis. Chromosome numbers are indicated following the species abbreviation. Different colors represent different chromosomes within each species. The twisted span connecting chromosome 2 of T. annulata and T. parva does not indicate an inversion.

FIG. 5.

Synteny between Cryptosporidium parvum and C. muris. Ticks = 100 kb. C. muris contigs are not assigned to chromosomes and are shown in order of designation. Chromosome numbers are indicated following the species abbreviation. Different colors represent different chromosomes within each species.

FIG. 6.

Limited synteny between Plasmodium falciparum and Theileria annulata. Ticks = 100 kb. This relationship is representative of the limited synteny between all Plasmodium and Piroplasm species. Chromosome numbers are indicated following the species abbreviation. Different colors represent different chromosomes within each species.

FIG. 7.

Distribution of species-specific, core, and multicopy genes. Each circle represents synteny between two species. Ticks = 100 kb. Highlights indicate the position of species-specific (red), core (black) and multicopy (blue) genes for (A) Plasmodium falciparum and P. vivax, (B) P. falciparum and P. berghei, (C) Babesia bovis and Theileria annulata, and (D) Cryptosporidium muris and C. parvum. Chromosome numbers are indicated following the species abbreviation. Different colors represent different chromosomes within each species.