Comparative Transcriptome Analysis of the Phototrophic Dinoflagellate Biecheleriopsis adriatica Grown Under Optimal Temperature and Cold and Heat Stress

Kang, Hee Chang; Jeong, Hae Jin; Park, Sang Ah; Ok, Jin Hee; You, Ji Hyun; Eom, Se Hee; Park, Eun Chong; Jang, Se Hyeon; Lee, Sung Yeon

doi:10.3389/fmars.2021.761095

Cited by 8 publications

(4 citation statements)

References 144 publications

(183 reference statements)

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“…Our multiple lines of omics data demonstrate a strong coordinated response, particularly under chronic heat stress, that reduces energy production and consumption via the reduction of photosynthesis, carbon fixation, and amino acid biosynthesis, resulting in a suppressed central metabolism and protein synthesis. These observations lend support to the results of earlier transcriptome studies of pelagic dinoflagellates 59, 60 .…”

Section: Discussionsupporting

confidence: 89%

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

Dougan

Deng

Woehlbrand

et al. 2022

Preprint

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Dinoflagellates are a large, ecologically important phylum of marine unicellular algae. Their huge genomes make it highly challenging to decipher the genetic basis of key processes such as harmful algal bloom (HAB) formation and response to warming oceans. To address these issues, we generated a high quality genome assembly from Prorocentrum cordatum, a globally abundant, HAB forming dinoflagellate. Our analyses demonstrate massive expansion of the gene inventory to 85,849 predicted genes, primarily driven by unusually long and frequent introns and dispersed duplicates enriched for bloom relevant functions. We find that cell yield is reduced at higher culture temperatures. To understand this response, we integrated transcriptome, proteome and metabolome data and identified both a global and a temperature specific heat-stress response. The underlying metabolic changes reflect damage to photosynthesis and central metabolism. The transcriptome data show that 25% of genes are differentially expressed under heat stress, with concomittant extensive RNA editing and alternative exon usage. Multi-codon genes and transcripts for HSP70 and RuBisCo suggest a polycistronic gene organisation. Our work represents the first genome based analysis of a red tide dinoflagellate and demonstrates that temperature resilience in P. cordatum is mediated by a unique genome structure and multi-level transcriptional regulation.

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Section: Discussionsupporting

confidence: 89%

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

Dougan

Deng

Woehlbrand

et al. 2022

Preprint

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Section: Discussionsupporting

confidence: 88%

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

Dougan,

Deng,

Wöhlbrand

et al. 2023

Genome Biol

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

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“…WGBS was performed in the dinoflagellates S. kawagutii and S. minutum at different temperature conditions, and global cytosine methylation levels provided similar results across samples of the same species, indicating the minimal effect of thermal stress on global methylation levels [ 78 ]. However, through a transcriptomic approach, it was observed that in the dinoflagellate Biecheleriopsis adriatica under cold stress, the “methylation” category had the highest difference between up- and down-regulated genes in gene ontology analysis, suggesting that cold stress may affect DNA methylation and gene expression in this microalga [ 128 ].…”

Section: Dna Methylation In Algae Response To Abiotic Stressmentioning

confidence: 99%

DNA Methylation in Algae and Its Impact on Abiotic Stress Responses

Ferrari

Muto

Bruno

et al. 2023

Plants

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Epigenetics, referring to heritable gene regulatory information that is independent of changes in DNA sequences, is an important mechanism involved both in organism development and in the response to environmental events. About the epigenetic marks, DNA methylation is one of the most conserved mechanisms, playing a pivotal role in organism response to several biotic and abiotic stressors. Indeed, stress can induce changes in gene expression through hypo- or hyper-methylation of DNA at specific loci and/or in DNA methylation at the genome-wide level, which has an adaptive significance and can direct genome evolution. Exploring DNA methylation in responses to abiotic stress could have important implications for improving stress tolerance in algae. This article summarises the DNA methylation pattern in algae and its impact on abiotic stress, such as heavy metals, nutrients and temperature. Our discussion provides information for further research in algae for a better comprehension of the epigenetic response under abiotic stress, which could favour important implications to sustain algae growth under abiotic stress conditions, often related to high biosynthesis of interesting metabolites.

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Comparative Transcriptome Analysis of the Phototrophic Dinoflagellate Biecheleriopsis adriatica Grown Under Optimal Temperature and Cold and Heat Stress

Cited by 8 publications

References 144 publications

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

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

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

DNA Methylation in Algae and Its Impact on Abiotic Stress Responses

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