Evolution of Mutator transposons in the genomes of worms

Abstract

Mutator-like elements (MULEs) were thought to be plant-specific, but research showed that MULEs are present in diverse eukaryotes including fungi, amoeba, worms etc. This study investigates the distribution, abundance, diversity and evolutionary dynamics of MULEs within the genomes of flatworms (Platyhelminthes), roundworms (Nematodes) and other worms (Acanthocephala, Annelida, Dicyemida and Nemertea). Multiples of divergent MULE families were identified and characterized with structural variability across the taxa. Few MULEs detected exhibit low Kimura divergence (KD) values, suggesting a recent transpositional capability. Structural analysis highlighted conserved catalytic domains (DDE), diverse terminal inverted repeats (TIRs) and their potential roles in shaping the genomes architecture. Functional implications of MULE prevalence in worms on host-parasitic interactions were explored. The evolutionary dynamics of MULEs within the taxa and their probable impact on the host species were inquired. This study discovered 113 types of MULE transposons (Tn) from 46 genomes of worm species researched. The MULEs detected are widely and unevenly distributed across Nematodes, Platyhelminthes, Acanthocephala, Annelida, Dicyemida and Nemertea. 25 MULE types harbour 358 full-length MULE copies and 284 intact MULE copies which encode functional transposases ≥300 amino acids (aa). The MULEs possess a wide size range, spanning from 1323 to 4819 base pairs (bp). They encode transposases (116-750 aa) with distinct TIRs (41-950 bp). Few MULEs detected have young insertion ages. This phenomenon indicates that these MULEs may be recent genome invaders with dynamic transposition energies. Transposons such as MULE-Mear-1, MULE-Meja-2 and MULE-Trsu-1 displayed multiple amplification waves reflecting their ongoing energetic transposition within the host. Only few transposons (<22 %) were discovered to harbour intact MULE copies ≥5. However, three MULE candidates were chosen for activity validation in human cells. The transposon (MULE-Apca-1) was designated as Acali for testing and evaluation. After a successful drug selection, the Acali transposase derived from the earthworm (Aporrectodea caliginosa) showed significant transposition activity relative to the hyperactive PB transposon. This study uncovered that MULEs are highly abundant in flatworms than roundworms and other worms. Nevertheless, MULE remnants exhibited wide distribution and diversity in Nematodes and Annelida (other worms) than Platyhelminthes. These findings emphasized the evolutionary importance of MULEs in worms with many new families yet to be discovered to enrich our understanding on the roles of DNA transposons in genome plasticity.

Keywords: Genetic; Plasticity; Taxa; Transposon.