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

ABSTRACT: Harmful algal blooms are induced largely by nutrient enrichment common in warm waters. An increasingly frequent phenomenon is the “red tide”: blooms of dinoflagellate microalgae that accumulate toxins lethal to other organisms in high doses. Here, we present the de novo assembled genome (~4.75 Gbp) of Prorocentrum cordatum, a globally abundant, bloom-forming dinoflagellate, and the associated transcriptome, proteome, and metabolome data from axenic cultures to elucidate the microalgal molecular responses to heat stress. We discovered, in a high-G+C genome with long introns and extensive genetic duplication, a complementary mechanism between RNA editing and exon usage that regulates dynamic expression and functional diversity of genes and proteins, and metabolic profiles that reflect reduced capacities in photosynthesis, central metabolism, and protein synthesis. These results based on multi-omics evidence demonstrate the genomic hallmark of a bloom-forming dinoflagellate, and how the complex gene structures combined with multi-level transcriptional regulation underpin concerted heat-stress responses.

INSTRUMENT(S):

ORGANISM(S): Prorocentrum Cordatum

SUBMITTER: Lars Wöhlbrand

LAB HEAD: Ralf Rabus

PROVIDER: PXD046193 | Pride | 2023-10-18

REPOSITORIES: Pride

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			Action	DRS
	P-mini_TempX_SG_1ug_Exp_20-C_smpl-1.1_GA1_01_355.d.zip	Other
	P-mini_TempX_SG_1ug_Exp_20-C_smpl-1.1_GA1_01_355.dat	Other
	P-mini_TempX_SG_1ug_Exp_20-C_smpl-1.2_GA2_01_357.d.zip	Other
	P-mini_TempX_SG_1ug_Exp_20-C_smpl-1.2_GA2_01_357.dat	Other
	P-mini_TempX_SG_1ug_Exp_20-C_smpl-1.3_GA3_01_359.d.zip	Other

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Project description:Dinoflagellates have evolved a nuclear organization unlike that of any other eukaryotic group. Recent studies find a predominance of post-transcriptional control of dinoflagellate gene expression. This study investigated regulation of the environmental stress response in the red tide dinoflagellate, Karenia brevis using an Agilent custom oligonucleotide microarray. K. brevis cultures were exposed to 5°C or 10°C heat shock, or three different sources of oxidative stress: 60 µM H2O2, 10 mM NaNO2, or 12 µM PbCl2 over acute time courses. Ribosomal genes, genes involved in RNA processing, translation, and chaperones were among the classes of genes consistently downregulated across treatments, although within these functional classes the same genes did not always respond to different stressors. Genes involved in the photosystem and mitochondrial and chloroplast ATP generation dominated the down-regulated genes. Heat shock and oxidative stress response genes were not induced under any treatment, even under conditions that resulted in decreased viability. We subsequently identified the presence of a trans-spliced leader sequence on many stress response gene transcripts, which suggests that they may be transcribed constitutively and their expression regulated at the level of translation. Cultures of were grown to mid-log phase. For each treatment, five replicate untreated control cultures and five replicate treated cultures were harvested at several time points following treatment. The following time courses were used: 5°C heat shock - 5, 15, 30, 60, and 240 min; 10°C heat shock - 60 min; 60 µM H2O2 - 5, 15, 30, 60, and 240 min; 10 mM NaNO2 -1, 4, and 7 hours; 12 µM PbCl2 -1, 4, and 7 hours. For each treatment, RNA was pooled from the controls and treated cultures at each timepoint. Two color arrays were then run comparing each the transcriptome at timepoint with the pooled control for that treatment. A technical dye swap array was run at each timepoint.

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

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