Genome plasticity in Paramecium bursaria revealed by population genomics

Abstract

Background Ciliates are an ancient and diverse eukaryotic group found in various environments. A unique feature of ciliates is their nuclear dimorphism, by which two types of nuclei, the diploid germline micronucleus (MIC) and polyploidy somatic macronucleus (MAC), are present in the same cytoplasm and serve different functions. During each sexual cycle, ciliates develop a new macronucleus in which newly fused genomes are extensively rearranged to generate functional minichromosomes. Interestingly, each ciliate species seems to have its way of processing genomes, providing a diversity of resources for studying genome plasticity and its regulation. Here, we sequenced and analyzed the macronuclear genome of different strains of Paramecium bursaria, a highly divergent species of the genus Paramecium which can stably establish endosymbioses with green algae. Results We assembled a high-quality macronuclear genome of P. bursaria and further refined genome annotation by comparing population genomic data. We identified several species-specific expansions in protein families and gene lineages that are potentially associated with endosymbiosis. Moreover, we observed an intensive chromosome breakage pattern that occurred during or shortly after sexual reproduction and contributed to highly variable gene dosage throughout the genome. However, patterns of copy number variation were highly correlated among genetically divergent strains, suggesting that copy number is adjusted by some regulatory mechanisms or natural selection. Further analysis showed that genes with low copy number variation among populations tended to function in basic cellular pathways, whereas highly variable genes were enriched in environmental response pathways. Conclusions We report programmed DNA rearrangements in the P. bursaria macronuclear genome that allow cells to adjust gene copy number globally according to individual gene functions. Our results suggest that large-scale gene copy number variation may represent an ancient mechanism for cells to adapt to different environments.

Genome editing excisase origins illuminated by somatic genome of Blepharisma

“…Recently it was reported that the Paramecium bursaria MAC genome is considerably more fragmented than those of other previously examined Paramecium species [44]. The DNA molecules from P. bursaria have thus also been classified as minichromosomes [44].…”

“…This places them between the “nanochromosomes” of ciliates like Oxytricha and Stylonychia , which typically encode single genes and a few kilobases long (Aeschlimann et al, 2014; Swart et al, 2013), and Paramecium tetraurelia and Tetrahymena thermophila MAC chromosomes which are hundreds of kilobases to megabases long (Aury et al, 2006; Sheng et al, 2020; Zagulski et al, 2004). The Paramecium bursaria MAC genome is considerably more fragmented than those of other previously examined Paramecium species, and have thus also been classified as minichromosomes (Cheng et al, 2020).…”

“…A minichromosomal architecture with pronounced telomere addition site variation Ciliate MAC genome architectures span from longer DNA molecules in the oligohymenophoreans Paramecium tetraurelia and Tetrahymena thermophila, which are more similar to conventional eukaryotic chromosomes, to numerous, predominantly single-gene nanochromosomes of spirotrichs like Oxytricha trifallax and Euplotes crassus [3]. The B. stoltei ATCC 30299 MAC genome organization (and like that of Paramecium bursaria [44]) lies between these two extremes with many minichromosomes representing numerous alternative telomere addition sites. This form of natural sequence heterogeneity creates significant new challenges for generating single representative consensus sequences, because genome assembly methods assume chromosome boundaries are generally consistent, as they are in multicellular eukaryote models, down to the terminology used to describe them [78].…”

“…This places them between the length of "nanochromosomes" of ciliates like Oxytricha and Stylonychia, which typically encode single genes and are on the order of a few kilobases long [39,40], and MAC chromosomes of Paramecium tetraurelia and Tetrahymena thermophila which are hundreds of kilobases to megabases long [41][42][43]. Recently it was reported that the Paramecium bursaria MAC genome is considerably more fragmented than those of other previously examined Paramecium species [44]. The DNA molecules from P. bursaria have thus also been classified as minichromosomes [44].…”

Phenotypic plasticity through disposable genetic adaptation in ciliates

“…Partial ploidy changes are a quick and reversible way to alter patterns of gene expression. In Paramecium bursaria copy number variation of macronuclear chromosomes is low for chromosomes harbouring housekeeping genes and high for those carrying environmental response genes [31]. Likewise, in the presence of toxic Cd 2+ , the copy number of a chromosome harbouring two metallothionein genes increased five-fold in T. thermophila [32].…”