Germline-limited transposon remnants foster somatic genome diversification

Transposable elements are mobile DNA sequences that propagate within genomes, often with deleterious effects on host fitness. Some organisms excise transposons from their somatic genomes via programmed DNA elimination yet paradoxically retain them in their germline. The evolutionary rationale for this selective retention remains poorly understood. To address this, we first set out to develop a germline enrichment method in Paramecium tetraurelia, since the somatic DNA is several hundred times more abundant than the transposon-rich germline. Our approach improved the germline assembly significantly by reducing the number of contigs from the previously published 26186 to just 179, close to the expected chromosomal count. Contrary to the view that the germline serves merely for transgenerational genome propagation, long-read sequencing of poly(A)+ RNA uncovered abundant coding transcripts derived from germline-limited DNA. Furthermore, we detected numerous modified somatic transcripts caused by incorporation of ultrashort transposon remnants from germline sequences. Notably, these insertions show a size bias that preserves open reading frames, consistent with translation mediated quality control. Together, our results suggest that the germ-soma nuclear dimorphism serves as an intrinsic system for the emergence of genome innovations and transcriptome diversification through the retention of germline-limited sequences.