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Sexual ancestors generated an obligate asexual and globally dispersed clone within the model diatom species Thalassiosira pseudonana.

ABSTRACT: Sexual reproduction roots the eukaryotic tree of life, although its loss occurs across diverse taxa. Asexual reproduction and clonal lineages persist in these taxa despite theoretical arguments suggesting that individual clones should be evolutionarily short-lived due to limited phenotypic diversity. Here, we present quantitative evidence that an obligate asexual lineage emerged from a sexual population of the marine diatom Thalassiosira pseudonana and rapidly expanded throughout the world's oceans. Whole genome comparisons identified two lineages with characteristics expected of sexually reproducing strains in Hardy-Weinberg equilibrium. A third lineage displays genomic signatures for the functional loss of sexual reproduction followed by a recent global colonization by a single ancestral genotype. Extant members of this lineage are genetically differentiated and phenotypically plastic, potentially allowing for rapid adaptation when they are challenged by natural selection. Such mechanisms may be expected to generate new clones within marginal populations of additional unicellular species, facilitating the exploration and colonization of novel environments, aided by exponential growth and ease of dispersal.

SUBMITTER: Koester JA

PROVIDER: S-EPMC6043606 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Sexual ancestors generated an obligate asexual and globally dispersed clone within the model diatom species Thalassiosira pseudonana.

Koester Julie A JA Berthiaume Chris T CT Hiranuma Naozumi N Parker Micaela S MS Iverson Vaughn V Morales Rhonda R Ruzzo Walter L WL Armbrust E Virginia EV

Scientific reports 20180712 1

Sexual reproduction roots the eukaryotic tree of life, although its loss occurs across diverse taxa. Asexual reproduction and clonal lineages persist in these taxa despite theoretical arguments suggesting that individual clones should be evolutionarily short-lived due to limited phenotypic diversity. Here, we present quantitative evidence that an obligate asexual lineage emerged from a sexual population of the marine diatom Thalassiosira pseudonana and rapidly expanded throughout the world's oce ...[more]

PMID: 30002405

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Project description:BACKGROUND:Silicon plays important biological roles, but the mechanisms of cellular responses to silicon are poorly understood. We report the first analysis of cell cycle arrest and recovery from silicon starvation in the diatom Thalassiosira pseudonana using whole genome microarrays. RESULTS:Three known responses to silicon were examined, 1) silicified cell wall synthesis, 2) recovery from silicon starvation, and 3) co-regulation with silicon transporter (SIT) genes. In terms of diatom cell wall formation, thus far only cell surface proteins and proteins tightly associated with silica have been characterized. Our analysis has identified new genes potentially involved in silica formation, and other genes potentially involved in signaling, trafficking, protein degradation, glycosylation and transport, which provides a larger-scale picture of the processes involved. During silicon starvation, an overrepresentation of transcription and translation related genes were up-regulated, indicating that T. pseudonana is poised to rapidly recover from silicon starvation and resume cell cycle progression upon silicon replenishment. This is in contrast to other types of limitation, and provides the first molecular data explaining the well-established environmental response of diatoms to grow as blooms and to out-compete other classes of microalgae for growth. Comparison of our data with a previous diatom cell cycle analysis indicates that assignment of the cell cycle specific stage of particular cyclins and cyclin dependent kinases should be re-evaluated. Finally, genes co-varying in expression with the SITs enabled identification of a new class of diatom-specific proteins containing a unique domain, and a putative silicon efflux protein. CONCLUSIONS:Analysis of the T. pseudonana microarray data has provided a wealth of new genes to investigate previously uncharacterized cellular phenomenon related to silicon metabolism, silicon's interaction with cellular components, and environmental responses to silicon.

Project description:BackgroundCP12 is a small chloroplast protein that is widespread in various photosynthetic organisms and is an actor of the redox signaling pathway involved in the regulation of the Calvin Benson Bassham (CBB) cycle. The gene encoding this protein is conserved in many diatoms, but the protein has been overlooked in these organisms, despite their ecological importance and their complex and still enigmatic evolutionary background.MethodsA combination of biochemical, bioinformatics and biophysical methods including electrospray ionization-mass spectrometry, circular dichroism, nuclear magnetic resonance spectroscopy and small X ray scattering, was used to characterize a diatom CP12.ResultsHere, we demonstrate that CP12 is expressed in the marine diatom Thalassiosira pseudonana constitutively in dark-treated and in continuous light-treated cells as well as in all growth phases. This CP12 similarly to its homologues in other species has some features of intrinsically disorder protein family: it behaves abnormally under gel electrophoresis and size exclusion chromatography, has a high net charge and a bias amino acid composition. By contrast, unlike other known CP12 proteins that are monomers, this protein is a dimer as suggested by native electrospray ionization-mass spectrometry and small angle X-ray scattering. In addition, small angle X-ray scattering revealed that this CP12 is an elongated cylinder with kinks. Circular dichroism spectra indicated that CP12 has a high content of α-helices, and nuclear magnetic resonance spectroscopy suggested that these helices are unstable and dynamic within a millisecond timescale. Together with in silico predictions, these results suggest that T. pseudonana CP12 has both coiled coil and disordered regions.ConclusionsThese findings bring new insights into the large family of dynamic proteins containing disordered regions, thus increasing the diversity of known CP12 proteins. As it is a protein that is more abundant in many stresses, it is not devoted to one metabolism and in particular, it is not specific to carbon metabolism. This raises questions about the role of this protein in addition to the well-established regulation of the CBB cycle. Choregraphy of metabolism by CP12 proteins in Viridiplantae and Heterokonta. While the monomeric CP12 in Viridiplantae is involved in carbon assimilation, regulating phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) through the formation of a ternary complex, in Heterokonta studied so far, the dimeric CP12 is associated with Ferredoxin-NADP reductase (FNR) and GAPDH. The Viridiplantae CP12 can bind metal ions and can be a chaperone, the Heterokonta CP12 is more abundant in all stresses (C, N, Si, P limited conditions) and is not specific to a metabolism. Video Abstract.

Dataset Information

Sexual ancestors generated an obligate asexual and globally dispersed clone within the model diatom species Thalassiosira pseudonana.

Publications

Sexual ancestors generated an obligate asexual and globally dispersed clone within the model diatom species Thalassiosira pseudonana.

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