Satellite-Like W-Elements: Repetitive, Transcribed, and Putative Mobile Genetic Factors with Potential Roles for Biology and Evolution of Schistosoma mansoni

Abstract

A large portion of animal and plant genomes consists of non-coding DNA. This part includes tandemly repeated sequences and gained attention because it offers exciting insights into genome biology. We investigated satellite-DNA elements of the platyhelminth Schistosoma mansoni, a parasite with remarkable biological features. S. mansoni lives in the vasculature of humans causing schistosomiasis, a disease of worldwide importance. Schistosomes are the only trematodes that have evolved separate sexes, and the sexual maturation of the female depends on constant pairing with the male. The schistosome karyotype comprises eight chromosome pairs, males are homogametic (ZZ), females heterogametic (ZW). Part of the repetitive DNA of S. mansoni are W-elements (WEs), originally discovered as female-specific satellite DNAs in the heterochromatic block of the W-chromosome. Based on new genome and transcriptome data, we performed a reanalysis of the W-element families (WEFs). Besides a new classification of 19 WEFs, we provide first evidence for stage-, sex-, pairing-, gonad-, and strain-specific/preferential transcription of WEs as well as their mobile nature, deduced from autosomal copies of full-length and partial WEs. Structural analyses suggested roles as sources of non-coding RNA like hammerhead ribozymes (HHRs), for which we obtained functional evidence. Finally, the variable WEF occurrence in different schistosome species revealed remarkable divergence. From these results we propose that WEs potentially exert enduring influence on the biology of S. mansoni. Their variable occurrence in different strains, isolates, and species suggests that schistosome WEs may represent genetic factors taking effect on variability and evolution of the family Schistosomatidae.

What We Talk About When We Talk About “Junk DNA”

“… Stitz et al (2021) used bioinformatics and omics data to characterize 19 W-element families (WEFs) in the genome of S. mansoni . Differently from the initial observation that W-elements (WEs) were restricted to the W chromosome, they found homologs of all WEFs in the autosomes (though only four WEFs had full-length copies).…”

“…Echoing ENCODE’s perspective in regard to the prominence of biochemical function, a recent study published in this journal analyzed new data for a class of genomic elements in S. mansoni to conclude that “it is tempting to speculate that more of the WE ‘junk-DNA’ than expected might be functional and relevant” ( Stitz et al 2021 ). An accompanying opinion piece highlights the redemption of repetitive elements from their “Junk DNA” status into “vital sources of [genomic] variation” ( McGrath 2021 ), which fits in the view that “the days of ‘Junk DNA’ are over” ( Stitz et al 2021 ).…”

Highlight—Epigenetics Virtual Issue: New Findings Amid Old Controversies

“…The role of TEs in epigenetic regulation is also discussed in a study led by Christoph Grunau and Christoph Grevelding on the human parasite Schistosoma mansoni ( Stitz et al 2021 ), a flatworm with a ZW sex chromosome system (in which males have two Z chromosomes and females have one Z and one W chromosome). Their study involved a reanalysis of repetitive W elements, which were originally thought to be found only on the W chromosome.…”

Highlight—“Junk DNA” No More: Repetitive Elements as Vital Sources of Flatworm Variation

“…“The days of ‘junk DNA’ are over,” according to Christoph Grunau and Christoph Grevelding, the senior authors of a new research article in Genome Biology and Evolution. Their study provides an in-depth look at an enigmatic superfamily of repetitive DNA sequences known as W elements in the genome of the human parasite Schistosoma mansoni ( Stitz et al 2021 ). Titled “ Satellite-like W elements: repetitive, transcribed, and putative mobile genetic factors with potential roles for biology and evolution of Schistosoma mansoni ,” the analysis reveals structural, functional, and evolutionary aspects of these elements and shows that, far from being “junk,” they may exert an enduring influence on the biology of S. mansoni .…”

“…The image is overlaid by a sample-distance matrix analysis showing the transcript occurrence of satellite DNA-like W element families transcribed at different levels across larval and adult stages. For more information, see Stitz et al (2021, Supplementary Fig. 6) .…”