Subtelomeric repeat expansion in Hydractinia symbiolongicarpus chromosomes

Abstract

Despite the striking conservation of animal chromosomes, their repetitive element complements are vastly diverse. Only recently, high quality chromosome-level genome assemblies enabled identification of repeat compositions along a broad range of animal chromosomes. Here, utilizing the chromosome-level genome assembly of Hydractinia symbiolongicarpus, a colonial hydrozoan cnidarian, we describe an accumulation of a single 372 bp repeat unit in the subtelomeric regions. Based on the sequence divergence, its partial affinity with the Helitron group can be detected. This sequence is associated with a repeated minisatellite unit of about 150 bp. Together, they account for 26.1% of the genome (126 Mb of the 483 Mb). This could explain the genome size increase observed in H. symbiolongicarpus compared with other cnidarians, yet distinguishes this expansion from other large cnidarian genomes, such as Hydra vulgaris, where such localized propagation is absent. Additionally, we identify a derivative of an IS3EU-like DNA element accumulated at the putative centromeric regions. Our analysis further reveals that Helitrons generally comprise a large proportion of H. symbiolongicarpus (11.8%). We investigated Helitron presence and distributions across several cnidarian genomes. We find that in Nematostella vectensis, an anthozoan cnidarian, Helitron-like sequences were similarly accumulated at the subtelomeric regions. All these findings suggest that Helitron derivatives are prone to forming chromosomal extensions in cnidarians through local amplification in subtelomeric regions, driving variable genome expansions within the clade.

Keywords: Helitron; Hydractinia symbiolongicarpus; Cnidarian; Genome expansion; IS3EU; Rolling-circle transposon; Subtelomere; Tandem repeats; Transposable elements.

Fig. 1

TE genome coverage in H. symbiolongicarpus genome. (a) Repeat landscape illustrating TE accumulation history for the H. symbiolongicarpus genome with the custom repetitive element library generated by RepeatModeler run with the default settings. The horizontal axis illustrates the Kimura substitution levels of repeat elements relative to their consensus sequences, indicating their ages. On the vertical axis, the graph depicts the genome coverage of each repeat family within the genome in Mb. Consequently, older repetitive elements appear toward the right side of the graph, while more recently active repetitive elements are positioned on the left. (b) Repeat landscape with the refined custom repetitive element library. (c) Genome coverage of TE superfamilies. (d) Genome coverage of TE families. (e) Copy number of TE families

Fig. 2

Subtelomeric and centromic expansions on H. symbiolongicarpus chromosomes. (a) Whole genome landscape of selected repeat localization. The first track represents all TEs, the second track represents HSymSHlR, and the third track depicts HSymSR. The fourth track shows HSymIS3EUlR. (b) Selected repeat localization on the chromosome 1. The regions highlighted by black horizontal lines (#1 and #2) are further emphasized in panel (c) and (d). (c) The regional plot on the chromosome 1 (region #1). (d) The regional plot on the chromosome 1 (region #2). The first to fourth tracks in panel (b), (c), and (d) are the same as in panels (a). (e) Distance to nearest gene. The boxplots illustrate the distance from the nearest gene for all TEs, HSymSHlR, HSymSR, and HSymIS3EUlR. The asterisks indicate that the median distance from the nearest gene is significantly greater compared to all TEs (p-value < 2.2e-16 for all asterisks, Wilcoxon rank-sum test). (f) The relationship between gene density and density of all TEs. (g) The relationship between gene density and HSymSHlR density

Fig. 3

Molecular phylogenetic analysis of HSymSHlR in H. symbiolongicarpus genome. (a) Sequence length distribution of HSymSHlR. (b) Sequence length distribution of HSymSR. (c) Multiple sequence alignment of all 177 HSymSHlR, with sequence lengths greater than 2.3 kb and less than 2.6 kb. (d) Multiple sequence alignment of 200 randomly selected HSymSR, with sequence lengths greater than 205 bp and less than 215 bp. The enlarged views of panels (c) and (d) are shown in Fig. S7. (e) Cladogram of a neighbor-joining tree of sequences from panel (c). Monophyletic groups formed by HSymSHlR sequences from the same chromosome arms are highlighted in red

Fig. 4

Helitrons in cnidarian genomes. (a) Cladogram of the six cnidarian species with their TE genome coverage and proportion of TEs in total TEs. (b) Proportion of TEs in total TEs across the six cnidarian species, with rows representing TEs, sorted by hierarchical clustering using the Euclidean distance and the Ward D2 methods. Columns represent species, all of which show varying amounts of Helitrons. (c) Sequence alignment of sequences similar to HSymHel from six cnidarians. The domain names are based on the analysis output from the NCBI Conserved Domain Search. (d) Genomic localization of Helitrons in Nematostella vectensis, highlighting the abundance of NveSHlR in subtelomeric regions. The first track shows the distribution of all TEs, the second track shows the distribution of NveSHlR, and the third track shows the distribution of IS3EU. Abbreviations of species names are as follows: NVE, Nematostella vectensis; AMI, Acropora millepora; RES, Rhopilema esculentum; HVI, Hydra viridissima; HVU, Hydra vulgaris; HSY, Hydractinia symbiolongicarpus