Environmentally induced plasticity of programmed DNA elimination boosts somatic variability inParamecium tetraurelia

Abstract

Can ecological changes impact somatic genome development? Efforts to resolve this question could reveal a direct link between environmental changes and somatic variability, potentially illuminating our understanding of how variation can surface from a single genotype under stress. Here, we tackle this question by leveraging the biological properties of ciliates. When Paramecium tetraurelia reproduces sexually, its polyploid somatic genome regenerates from the germline genome through a developmental process that involves the removal of thousands of ORF-interrupting sequences known as internal eliminated sequences (IESs). We show that exposure to nonstandard culture temperatures impacts the efficiency of this process of programmed DNA elimination, prompting the emergence of hundreds of incompletely excised IESs in the newly developed somatic genome. These alternative DNA isoforms display a patterned genomic topography, impact gene expression, and might be inherited transgenerationally. On this basis, we conclude that environmentally induced developmental thermoplasticity contributes to genotypic diversification in Paramecium.

Prolonged exposure to constant environmental conditions prompts nonrandom genetic variation

“…Alternatively, somatic IESs may have accrued preferentially in down-regulated genes. At any rate, the negative scaling between IES retention levels and gene expression in both the control stock d12 (Vitali et al 2019) and stock 51 (Kendall’s τ = −0.176, P <0.0001) further supports the relationship between developmental variation and somatic gene expression in P. tetraurelia .…”

“…It also predicts that the MA lines and the control stocks may have undergone divergent changes in gene expression level over the ∼4-year long MA experiment. To test this, we leveraged the transcriptomes of the control stocks 51 (Arnaiz et al 2017) and d12 (Vitali et al 2019) obtained at standard (MA experiment-like) cultivation conditions. We found that genes with reduced levels of expression in the control stocks preferentially accumulate somatic IESs ( Figure 3D ), consistent with previous reports (Arnaiz et al 2012; Ferro et al 2015; Vitali et al 2019) .…”

“…To test this, we leveraged the transcriptomes of the control stocks 51 (Arnaiz et al 2017) and d12 (Vitali et al 2019) obtained at standard (MA experiment-like) cultivation conditions. We found that genes with reduced levels of expression in the control stocks preferentially accumulate somatic IESs ( Figure 3D ), consistent with previous reports (Arnaiz et al 2012; Ferro et al 2015; Vitali et al 2019) . The opposite is true for the MA lines, where an excess of highly expressed genes retain IESs relative to the control stocks (two proportions Z test, P < 0.0001).…”

“…In P. tetraurelia , the development of a new somatic nucleus from the zygotic nucleus involves DNA amplification (from 2 n to ∼860 n (Woodard et al 1961) ) and rearrangements including the elimination of ∼45,000 intervening germline DNA regions termed Internal Eliminated Sequences (IESs) (Betermier 2004; Duharcourt et al 2009; Arnaiz et al 2012) . This process of Programmed DNA Elimination (PDE) is not foolproof, allowing newly developed somatic genomes to retain IESs (Duret et al 2008; Catania et al 2013; Vitali et al 2019) . In a typical deep-sequencing study, IES retention is limited to a few hundred somatic loci and mainly involves ≤ 5% of the ∼860 copies per locus when P. tetraurelia is cultured under standard conditions ( Table S1 ).…”

“…In a typical deep-sequencing study, IES retention is limited to a few hundred somatic loci and mainly involves ≤ 5% of the ∼860 copies per locus when P. tetraurelia is cultured under standard conditions ( Table S1 ). However, the cultivation environment can significantly perturb PDE in P. tetraurelia , generating DNA variation that might be heritable and potentially adaptive (Vitali et al 2019) .…”