Cross-Generational Effects and Non-random Developmental Response to Temperature Variation in Paramecium

Abstract

Unicellular organisms such as ciliates are largely neglected in research on adaptive developmental plasticity, although their nuclear dualism offers ideal circumstances to study development outside an embryonic context. Here, we gain first insights into the ability of the ciliate Paramecium to develop potentially adaptive phenotypic changes in response to early-life adversity. We show that, upon exposure to unconventional culture temperatures, germ line-to-soma differentiation gives rise to coordinated molecular changes that may help attune the number of functional gene copies to the new external conditions. The non-random somatic heterogeneity that developmental plasticity generates is largely epigenetically controlled, shaped by the parental experience, and may prompt a stress response. These findings establish Paramecium as a new model system to study the molecular basis and evolutionary significance of developmental plasticity. In echoing previous indications in mammals, they call for an incorporation of intergenerational effects in adaptation studies.

Fifty Generations of Amitosis: Tracing Asymmetric Allele Segregation in Polyploid Cells with Single-Cell DNA Sequencing

“…Somatic IESs may be viewed as AT-rich insertions (somatic mutations) that occur naturally in Paramecium following somatic genome development [ 33 , 36 , 37 , 38 , 39 ]. To determine whether the uncovered biases of scDNA-seq ( Figure 1 and Table 1 ) limit our ability to detect somatic IESs, we compared the somatic genomes obtained from mass culture and single cells.…”

“…Although IESs are, for the most part, perfectly removed from the newly developed somatic genome, some are incompletely excised—in the order of a few hundreds in standard cultivation conditions [ 36 ]. These retained elements, which we termed somatic IESs, interrupt a variable fraction (henceforth retention levels) of the total number of macronuclear DNA copies [ 33 , 36 , 37 , 38 , 39 ]. The retention levels of somatic IESs provide a measurable molecular marker to assess the random assortment of segregating alleles in Paramecium (and other ciliates).…”

Fifty generations of amitosis: tracing asymmetric allele segregation in polyploid cells with single-cell DNA sequencing

“…Somatic IESs may be viewed as AT-rich insertions that occur naturally in Paramecium following somatic genome development (Arnaiz et al 2012; Catania et al 2013; Duret et al 2008; Hagen et al 2020; Vitali et al 2019) . Detection of these somatic IESs requires pervasive and deep genome coverage as mutant alleles (IES + ) are scattered across the genome and can be retained in a variable fraction of the polyploid somatic nucleus, coexisting with their wild-type alleles (IES − ).…”

“…However, Preer and Nyberg cautioned that higher ploidy levels (>>860n) would still be compatible with random segregation of individual somatic chromosomes (Nyberg 1976; Preer 1976). Re-examining the impact that amitosis may have on the somatic variability of Paramecium is relevant and particularly timely as it is now clear that potentially heritable somatic variability in Paramecium can spark from a fully homozygous state as a consequence of incomplete excision of germline DNA sequences (Hagen et al 2020; Vitali et al 2019) .…”

“…Although IESs are, for the most part, perfectly removed from the newly developed somatic genome, some are incompletely excised—in the order of a few hundreds at standard cultivation conditions (Vitali, Hagen, and Catania 2019) . These retained elements, which we termed somatic IESs, interrupt a variable fraction (henceforth retention levels) of the total number of macronuclear DNA copies (Arnaiz et al 2012; Catania et al 2013; Duret et al 2008; Hagen, Vitali, and Catania 2020; Vitali et al 2019) . The retention levels of somatic IESs provide a measurable molecular marker to assess the random assortment of segregating alleles in Paramecium .…”