Phenotypic plasticity through disposable genetic adaptation in ciliates

Verdonck, Rik; Legrand, Delphine; Jacob, Staffan; Piégay, Hervé

doi:10.1016/j.tim.2021.06.007

“…In our system, sex may have immediate and strong fitness consequences due to the nuclear dimorphism typical of all ciliates. Aside from creating novel genetic variants (in the germline micronucleus), sexual reproduction also involves the recreation of a new somatic macronucleus and thereby the loss of any (somatic) adaptation acquired during asexual life (44).…”

Section: Discussionmentioning

confidence: 99%

Predicting evolution in experimental range expansions of an aquatic model system

Zilio

¹

,

Krenek²,

Gougat-Barbera

³

et al. 2022

Preprint

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Predicting range expansion dynamics is challenging for fundamental and applied research, especially if ecological and evolutionary processes occur over similar time scales. We assessed the predictability of evolutionary outcomes in laboratory range expansions of the ciliate Paramecium caudatum. Experimental range core and front treatments were recreated in a predictive mathematical model, parametrized with dispersal and growth data of the 20 founder strains. Short-term evolution from standing genetic variation was driven by selection for dispersal at the front and general selection for growth rate in all treatments. The quantitative match between predicted and observed trait changes was mirrored by genetic divergence between treatments, with the repeated fixation of strains identified as most likely winners in our model. Long-term evolution in range front lines produced a dispersal syndrome (competition - colonisation trade-off). Our work suggests that short-term evolution at range fronts can follow predictable trajectories, based on few key parameters.

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“…Those cells belonging to the same developed MAC offer high methodological facility (no need to separate MICs from MACs) and statistical power (all mutations are de facto MAC- de novo -SNPs) to estimate the time since the last sexual event, and thus the duration of asexual phase in nature. Although sexual reproduction is supposed to be frequent in natural populations of T. thermophila [62], its influence on population’s persistence relative to somatic selection during asexual phases is largely unknown [30]. Other eco-evolutionary perspectives would be to barcode tetrahymine cells issued from different environments using both SNPs and distribution of indels at MDS junctions to link fitness advantages (for instance better competitive or dispersal abilities) to these different sources of genomic variations.…”

Section: Resultsmentioning

confidence: 99%

“…In the case of T. thermophila (∼45n), the latter implies that, in the absence of selection, each cell lineage fixes 99% of its loci in ∼200 asexual generations. Amitosis offers an unusual panel of somatic genomic variants on which selection can act at each asexual generation [30]. For instance, in the presence of toxic cadmium ions, both chromosome copy number variation and paralogous expansion of metallothionein have been observed in T. thermophila in a few asexual generations [31].…”

Section: Introductionmentioning

confidence: 99%

“…For instance, in the presence of toxic cadmium ions, both chromosome copy number variation and paralogous expansion of metallothionein have been observed in T. thermophila in a few asexual generations [31]. The evolutionary origin of this somatic genome remains unclear but a role in the domestication of transposable elements [32–34], as well as a role in phenotypic plasticity through somatic selection [30], have been proposed.…”

Section: Introductionmentioning

confidence: 99%

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The macronuclear genomic landscape withinTetrahymena thermophila

Derelle,

Verdonck,

Jacob

et al. 2023

Preprint

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The extent of intraspecific genomic variation is key to understanding species evolutionary history, including recent adaptive shifts. Intraspecific genomic variation remains poorly explored in eukaryotic microorganisms, especially in the nuclear dimorphic ciliates, despite their fundamental role as laboratory model systems and their ecological importance in many ecosystems. We sequenced the macronuclear genome of 22 laboratory strains of the oligohymenophoranTetrahymena thermophila, a model species in both cellular biology and evolutionary ecology. We explored polymorphisms at the junctions of programmed eliminated sequences, and reveal their utility to barcode very closely related cells. As for other species of the genusTetrahymena, we confirm micronuclear centromeres as gene diversification centres inT. thermophila, but also reveal a two-speed evolution in these regions. In the rest of the genome, we highlight recent diversification of genes encoding for extracellular proteins and cell adhesion. We discuss all these findings in relation with ciliate’s ecology and cellular characteristics.Impact StatementThis is the first study of population genomics in the ciliateTetrahymena thermophila. This bacterivore species plays an important role in aquatic trophic chains and is widely used as a model in cell and molecular biology, ecology, evolution or toxicology. As all ciliates, it contains a germline micronucleus and a somatic macronucleus. Sequencing of the macronucleus reveals that the centromeric region of the micronucleus are simultaneously a region of new gene diversification, as observed in otherTetrahymenaspecies, and a region containing highly conserved genes. The results also confirm that the formation of the macronucleus from the micronucleus is highly imprecise. Interestingly, this process generates a genomic barcode that can discriminate cells derived from a given sexual reproduction event, allowing to study more finely population dynamics/history in nature.Data summaryAll data are fully provided in Supplementary Materials. The raw data of the 22Tetrahymenagenomes have been deposited in the Sequence Read Archive (https://www-ncbi-nlm-nih-gov.inee.bib.cnrs.fr/bioproject/PRJNA1012331). Accession numbers are listed in Table S1 (available in the online version of this article).

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“…For instance, in the presence of toxic cadmium ions, both chromosome copy number variation and paralogous expansion of metallothionein have been observed in T. thermophila in a few asexual generations [31]. The evolutionary origin of this somatic genome remains unclear but a role in the domestication of transposable elements [32][33][34], as well as a role in phenotypic plasticity through somatic selection [30], have been proposed. Several ciliate MAC reference genomes have been published, including of species of the genera Tetrahymena [35], Paramecium [29,36], Oxytricha [37] or the heterotrichean Stentor [38].…”

Section: Introductionmentioning

confidence: 99%

The macronuclear genomic landscape within Tetrahymena thermophila

Derelle,

Verdonck,

Jacob

et al. 2024

Microbial Genomics

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The extent of intraspecific genomic variation is key to understanding species evolutionary history, including recent adaptive shifts. Intraspecific genomic variation remains poorly explored in eukaryotic micro-organisms, especially in the nuclear dimorphic ciliates, despite their fundamental role as laboratory model systems and their ecological importance in many ecosystems. We sequenced the macronuclear genome of 22 laboratory strains of the oligohymenophoran Tetrahymena thermophila, a model species in both cellular biology and evolutionary ecology. We explored polymorphisms at the junctions of programmed eliminated sequences, and reveal their utility to barcode very closely related cells. As for other species of the genus Tetrahymena, we confirm micronuclear centromeres as gene diversification centres in T. thermophila, but also reveal a two-speed evolution in these regions. In the rest of the genome, we highlight recent diversification of genes coding for extracellular proteins and cell adhesion. We discuss all these findings in relation to this ciliate’s ecology and cellular characteristics.

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Phenotypic plasticity through disposable genetic adaptation in ciliates

Cited by 10 publications

References 89 publications

Predicting evolution in experimental range expansions of an aquatic model system

Predicting evolution in experimental range expansions of an aquatic model system

The macronuclear genomic landscape withinTetrahymena thermophila

The macronuclear genomic landscape within Tetrahymena thermophila

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