Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate

Genome biology, Journal Year: 2023, Volume and Issue: 24(1)

Published: Nov. 23, 2023

Abstract Background “Red tides” are harmful algal blooms caused by dinoflagellate microalgae that accumulate toxins lethal to other organisms, including humans via consumption of contaminated seafood. These driven a combination environmental factors nutrient enrichment, particularly in warm waters, and increasingly frequent. The molecular, regulatory, evolutionary mechanisms underlie the heat stress response these bloom-forming species remain little understood, due part limited genomic resources from dinoflagellates, complicated large sizes genomes, exhibiting features atypical eukaryotes. Results We present de novo assembled genome (~ 4.75 Gbp with 85,849 protein-coding genes), transcriptome, proteome, metabolome Prorocentrum cordatum , globally abundant, dinoflagellate. Using axenic cultures, we study molecular underpin stress, which is relevant current ocean warming trends. first evidence complementary interplay between RNA editing exon usage regulates expression functional diversity biomolecules, reflected reduction photosynthesis, central metabolism, protein synthesis. results reveal signatures post-transcriptional regulation for time pelagic Conclusions Our multi-omics analyses uncover an important species, complex gene structures large, high-G+C genome, combined multi-level transcriptional regulation. dynamics regulatory may explain how dinoflagellates diversified become some most ecologically successful organisms on Earth.

Language: Английский

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Developing model systems for dinoflagellates in the post‐genomic era

Journal of Phycology, Journal Year: 2023, Volume and Issue: 59(5), P. 799 - 808

Published: Sept. 1, 2023

Dinoflagellates are a diverse group of eukaryotic microbes that ubiquitous in aquatic environments. Largely photosynthetic, they encompass symbiotic, parasitic, and free-living lineages with broad spectrum trophism. Many taxa can produce bioactive secondary metabolites such as biotoxins, some which cause harmful algal blooms. In contrast, most symbiotic species crucial for sustaining coral reef health. The year 2023 marked decade since the first genome data dinoflagellates became available. growing genome-scale resources these highlighting their remarkable evolutionary genomic complexities. Here, we discuss prospect developing dinoflagellate models using criteria accessibility, tractability, resources, research support, promise. Moving forward post-genomic era, argue development fit-to-purpose tailor to specific biological contexts, one-size-fits-all model is inadequate encapsulating complex biology, ecology, history dinoflagellates.

Language: Английский

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Evidence for adaptive morphological plasticity in the Caribbean coral, Acropora cervicornis

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(49)

Published: Nov. 28, 2022

Genotype-by-environment interactions (GxE) indicate that variation in organismal traits cannot be explained by fixed effects of genetics or site-specific plastic responses alone. For tropical coral reefs experiencing dramatic environmental change, identifying the contributions genotype, environment, and GxE on performance will vital for both predicting persistence developing restoration strategies. We quantified impacts G, E, morphology survival endangered coral, Acropora cervicornis, through an situ transplant experiment exposing common garden (nursery)-raised clones ten genotypes to nine reef sites Florida Keys. By fate-tracking outplants over one year with colony-level 3D photogrammetry, we uncovered significant size, shape, survivorship, indicating no universal winner exists terms colony performance. Rather than differences mean trait values, found individual-level morphological plasticity is adaptive most individuals also exhibited fastest growth highest survival. This indicates may continue evolve, influencing success A. cervicornis resulting communities a changing climate. As focal are active sites, knowledge phenotype important predictor can directly applied planning. Taken together, these results establish as system studying ecoevolutionary dynamics phenotypic inform genetic- environment-based strategies restoration.

Language: Английский

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Facultative lifestyle drives diversity of coral algal symbionts

Trends in Ecology & Evolution, Journal Year: 2023, Volume and Issue: 39(3), P. 239 - 247

Published: Nov. 10, 2023

The photosynthetic symbionts of corals sustain biodiverse reefs in nutrient-poor, tropical waters. Recent genomic data illuminate the evolution coral under genome size constraints and suggest that retention facultative lifestyle, widespread among these algae, confers a selective advantage when compared with strict symbiotic existence. We posit symbiosis is analogous to 'bioreactor' selects winner genotypes allows them rise high numbers sheltered habitat prior release by host. Our observations lead novel hypothesis, 'stepping-stone model', which predicts local adaptation both free-living stages, stepwise fashion, accelerates alga diversity origin endemic strains species.

Language: Английский

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Synergistic response to climate stressors in coral is associated with genotypic variation in baseline expression

Proceedings of the Royal Society B Biological Sciences, Journal Year: 2024, Volume and Issue: 291(2019)

Published: March 27, 2024

As environments are rapidly reshaped due to climate change, phenotypic plasticity plays an important role in the ability of organisms persist and is considered especially acclimatization mechanism for long-lived sessile such as reef-building corals. Often, this a single genotype display multiple phenotypes depending on environment modulated by changes gene expression, which can vary response environmental via two mechanisms: baseline expression plasticity. We used transcriptome-wide profiling eleven genotypes common-gardened Acropora cervicornis explore genotypic variation thermal acidification stress, both individually combination. show that combination these stressors elicits synergistic response, stress variation. Additionally, we demonstrate frontloading large module coexpressed genes associated with greater retention algal symbionts under combined stress. These results illustrate individuals change even when have shared histories, affecting their performance future scenarios.

Language: Английский

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Alignment-Free Analysis of Whole-Genome Sequences From Symbiodiniaceae Reveals Different Phylogenetic Signals in Distinct Regions

Frontiers in Plant Science, Journal Year: 2022, Volume and Issue: 13

Published: April 26, 2022

Dinoflagellates of the family Symbiodiniaceae are predominantly essential symbionts corals and other marine organisms. Recent research reveals extensive genome sequence divergence among taxa high phylogenetic diversity hidden behind subtly different cell morphologies. Using an alignment-free approach based on sub-sequences fixed length k (i.e. k-mers), we assessed signal whole-genome sequences from 16 (including genera Symbiodinium, Breviolum, Cladocopium, Durusdinium Fugacium) two strains Polarella glacialis as outgroup. Based trees inferred k-mers in distinct genomic regions repeat-masked sequences, protein-coding introns repeats) protein associated with DNA encoded amino acids is largely consistent phylogeny established markers, such large subunit rRNA. The (introns exhibit signals, supporting expected differential evolutionary pressure acting these regions. Our analysis conserved core revealed prevalence (>95% 23-mers all 18 genomes) annotated repeats non-genic genomes. We observed 180 repeat types that significantly enriched genomes symbiotic versus free-living Symbiodinium taxa, suggesting enhanced activity transposable elements linked to lifestyle. provide evidence representation phylogenies dynamic networks enhances ability generate new hypotheses about evolution Symbiodiniaceae. These results demonstrate potential methods a scalable for inferring comprehensive, unbiased dinoflagellates more broadly microbial eukaryotes.

Language: Английский

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Global phylogenomic assessment of Leptoseris and Agaricia reveals substantial undescribed diversity at mesophotic depths

BMC Biology, Journal Year: 2023, Volume and Issue: 21(1)

Published: June 26, 2023

Abstract Background Mesophotic coral communities are increasingly gaining attention for the unique biological diversity they host, exemplified by numerous mesophotic fish species that continue to be discovered. In contrast, many of photosynthetic scleractinian corals observed at depths assumed depth-generalists, with very few characterised as mesophotic-specialists. This presumed lack a specialised community remains largely untested, phylogenetic studies on have rarely included samples and long suffered from resolution issues associated traditional sequence markers. Results Here, we used reduced-representation genome sequencing conduct phylogenomic assessment two dominant genera plating in Indo-Pacific Western Atlantic, respectively, Leptoseris Agaricia. While these genome-wide phylogenies broadly corroborated morphological taxonomy, also exposed deep divergences within undescribed across current taxonomic species. Five eight focal consisted least sympatric genetically distinct lineages, which were consistently detected different methods. Conclusions The repeated observation divergent lineages highlights there may more mesophotic-specialist than currently acknowledged an urgent this unstudied is warranted.

Language: Английский

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Chemical mutagenesis and thermal selection of coral photosymbionts induce adaptation to heat stress with trait trade‐offs

Evolutionary Applications, Journal Year: 2023, Volume and Issue: 16(9), P. 1549 - 1567

Published: Aug. 19, 2023

Despite the relevance of heat-evolved microalgal endosymbionts to coral reef restoration, date, few Symbiodiniaceae strains have been thermally enhanced via experimental evolution. Here, we investigated whether thermal tolerance can be increased through chemical mutagenesis followed by selection. Strains Durusdinium trenchii, Fugacium kawagutii and Symbiodinium pilosum were exposed ethyl methanesulfonate induce random mutagenesis, then underwent selection at high temperature (31/33°C). After 4.6-5 years evolution, in vitro these was assessed reciprocal transplant experiments ambient (27°C) elevated (31/35°C) temperatures. Growth, photosynthetic efficiency, oxidative stress nutrient use measured compare between strains. Heat-evolved D. F. S. all exhibited efficiency under stress. However, trade-offs growth rates observed for trenchii lineage both Reduced phosphate nitrate uptake lineages, respectively, suggest alterations nutrition resource usage allocation processes may occurred. Increased strain indicate that evolution resulted further this species. These findings deepen our understanding physiological responses cultures their capacity adapt The new developed here beneficial restoration efforts if conferred hospite.

Language: Английский

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Massive genome reduction occurred prior to the origin of coral algal symbionts

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: March 25, 2023

Abstract Dinoflagellates in the Family Symbiodiniaceae (Order Suessiales) are diverse, predominantly symbiotic lineages that associate with taxa such as corals and jellyfish. Their ancestor is believed to have been free-living, establishment of symbiosis (i.e., symbiogenesis) hypothesised occurred multiple times during evolution. Among taxa, genus Effrenium an early diverging, free-living lineage phylogenetically positioned between two robustly supported groups genera within which emerged. The lack symbiogenesis suggests ancestral features may retained this lineage. Here we present de novo assembled genomes associated transcriptome data from three isolates voratum . We compared (1.2-1.9 Gbp size) gene those 16 other outgroup dinoflagellates. Surprisingly, find genome reduction, often a lifestyle, predates origin Symbiodiniaceae. postulate adaptation extreme habitat (e.g., Polarella glacialis ) or life oligotrophic conditions resulted Suessiales having haploid size < 2Gbp, was (or reduced) among all extant algae Nonetheless, our reveal lifestyle distinguishes vis-à-vis their longer introns, more-extensive mRNA editing, fewer (∼30%) lineage-specific families, lower (∼10%) level pseudogenisation. These results demonstrate how reduction versus lifestyles intersect, driven diversification evolution

Language: Английский

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Gene duplication is the primary driver of intraspecific genomic divergence in coral algal symbionts

Open Biology, Journal Year: 2023, Volume and Issue: 13(9)

Published: Sept. 1, 2023

Dinoflagellates in the order Suessiales include family Symbiodiniaceae, which have essential roles as photosymbionts corals, and their cold-adapted sister group, Polarella glacialis. These diverse taxa exhibit extensive genomic divergence, although genomes are relatively small (haploid size < 3 Gbp) when compared with most other free-living dinoflagellates. Different strains of Symbiodiniaceae form symbiosis distinct hosts different regimes gene expression, but intraspecific whole-genome divergence is poorly understood. Focusing on three species (the Effrenium voratum symbiotic Symbiodinium microadriaticum Durusdinium trenchii) outgroup P. glacialis, for data from multiple isolates available, we assessed respect to sequence structure. Our analysis, based alignment alignment-free methods, revealed a greater extent than results underscore role duplication generating functional innovation, prevalence tandemly duplicated single-exon genes observed symbionts. demonstrate remarkable dinoflagellates under constraint reduced genome sizes, shaped by genetic duplications symbiogenesis events during diversification Symbiodiniaceae.

Language: Английский

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