Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection

Abstract

Background Chromosome-level assemblies are indispensable for accurate gene prediction, synteny assessment, and understanding higher-order genome architecture. Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here, we present the complete genome of the tapeworm Hymenolepis microstoma, providing a reference quality, end-to-end assembly that represents the first fully assembled genome of a spiralian/lophotrochozoan, revealing new insights into chromosome evolution. Results Long-read sequencing and optical mapping data were added to previous short-read data enabling complete re-assembly into six chromosomes, consistent with karyology. Small genome size (169 Mb) and lack of haploid variation (1 SNP/3.2 Mb) contributed to exceptionally high contiguity with only 85 gaps remaining in regions of low complexity sequence. Resolution of repeat regions reveals novel gene expansions, micro-exon genes, and spliced leader trans-splicing, and illuminates the landscape of transposable elements, explaining observed length differences in sister chromatids. Syntenic comparison with other parasitic flatworms shows conserved ancestral linkage groups indicating that the H. microstoma karyotype evolved through fusion events. Strikingly, the assembly reveals that the chromosomes terminate in centromeric arrays, indicating that these motifs play a role not only in segregation, but also in protecting the linear integrity and full lengths of chromosomes. Conclusions Despite strong conservation of canonical telomeres, our results show that they can be substituted by more complex, species-specific sequences, as represented by centromeres. The assembly provides a robust platform for investigations that require complete genome representation.

Step-by-Step Evolution of Telomeres: Lessons from Yeasts

“…This observation further underlines a possible functional and evolutionary relationship between centromeres and telomeres ( Villasante et al. 2007 ) and suggests that under specific conditions, one type of the repetitive DNA element can be replaced by the other ( Olson et al. 2020 ).…”

“…1999 ], 28 Tribolium castaneum [ Osanai et al. 2006 ], 29 Hymenolepis microstoma [ Olson et al. 2020 ], 30 Drosophila melanogaster [ Levis et al.…”

“…Specifically, in contrast to most flatworms, whose telomeres are composed of 5′-TTAGGG-3′ repeats ( Bombarová et al. 2009 ), some chromosomal ends of the tapeworm Hymenolepis microstoma terminate with extremely long (median unit length of 179 nt) repeats, which exhibit several traits typical for centromeric sequences ( Olson et al. 2020 ).…”

SLIDR and SLOPPR: Flexible identification of spliced leadertrans-splicing and prediction of eukaryotic operons from RNA-Seq data

“…SLIDR is designed as an assembly tool that constructs initial putative SLs directly from 5’ read tails that remain unaligned (“soft-clipped”) after alignment to a genome or transcriptome reference [33]. Unlike other methods, SLIDR then implements several optional plausibility checks based on functional nucleotide motifs in the SL RNA molecule, i.e., splice donor and acceptor sites, Sm binding motifs and several stem loops [2, 38].…”

SLIDR and SLOPPR: flexible identification of spliced leader trans-splicing and prediction of eukaryotic operons from RNA-Seq data

“…High-throughput RNA-Seq data is an attractive alternative resource that may often already exist for the focal organism. Novel SLs can, in principle, be identified from overrepresented 5′ tails extracted directly from RNA-Seq reads [32,33]. Based on this idea, the SLFinder pipeline assembles putative SLs from overrepresented k-mers at transcript ends and uses these SLs as guides for searching potential SL RNA genes in genome assemblies [34].…”