Expansion of a single Helitron subfamily in Hydractinia symbiolongicarpus suggests a shared mechanism of cnidarian chromosomal extension

Abstract

Helitrons are rolling-circle transposons that amplify through rolling-circle replication mechanism. Since Helitrons were relatively recently identified, their impact on genome evolution is still not fully understood. Here, we describe that a single Helitron subfamily specifically accumulates in the subtelomeric regions of Hydractinia symbiolongicarpus, a colonial hydrozoan cnidarian. Based on the sequence divergence, it is suggested that the Helitron subfamily underwent a burst of activity in the species recent history. Additionally, there is a IS3EU DNA element accumulation at the putative centromeric regions, as well as minisatellite sequences of approximately 200 bp in length extending from the telomere-side end of the Helitron towards the telomere. Phylogenetic analysis of Helitrons in the H. symbiolongicarpus genome suggests that the Helitrons underwent local propagation at the subtelomeric regions. The single Helitron subfamily, along with the consecutive minisatellite, accounts for 26.1% of the genome coverage (126 Mb of the 483 Mb genome), which collectively contribute to the genome size increase observed in H. symbiolongicarpus compared with other cnidarians. Homologous sequences of Helitron in H. symbiolongicarpus were identified in the genomes of other cnidarians, suggesting that Helitrons in hydractinia were present in at least the common ancestor of Cnidaria. Furthermore, in Nematostella vectensis, an anthozoan cnidarian, Helitrons were also accumulated at the subtelomeric regions. All these findings suggest that Helitrons constitute a common cnidarian mechanism of chromosomal extension through local amplification in subtelomeric regions, driving diverse genome expansions within the clade.