The tiny germline chromosomes of Paramecium aurelia have an exceptionally high recombination rate and are capped by a new class of Helitrons.
Paramecia belong to the ciliate phylum of unicellular eukaryotes characterized by nuclear dimorphism. A diploid germline micronucleus (MIC) transmits genetic information across sexual generations. A polyploid transcriptionally active somatic macronucleus (MAC) develops at each sexual generation from a copy of the MIC through programmed DNA elimination (PDE) of > 30% of germline DNA. PDE requires the domesticated PiggyMac (Pgm) transposase. Assembly of Paramecium germline genomes has presented an enormous challenge owing to the difficulty of MIC isolation. Here we report chromosome-scale short-read MIC assemblies for 7 species from the P. aurelia species complex. We discovered a novel clade of Helitrons, with 9-10 kb transposase ORFs under purifying selection, that have remained active in all P. aurelia lineages. A long-read assembly for P. tetraurelia together with a genetic linkage map provided a nearly telomere-to-telomere assembly. The genome consists of tiny (300 kb – 1.2 Mb) and numerous (~160) germline chromosomes with the highest recombination rate ever reported for a eukaryote (420 cM/Mb). The ends of the chromosomes consist of Helitrons inserted in telomeric C4A2 repeats, forming a distinct genomic compartment that is eliminated very early during MAC development by an unknown, Pgm-independent, mechanism.