The responses of harmful dinoflagellate Karenia mikimotoi to simulated ocean acidification at the transcriptional level

The HAB-forming, toxic dinoflagellate Karenia mikimotoi, previously found to benefit from ocean acidification (OA), was cultivated to investigate its transcriptional response to simulated OA for 30 generations. Batch cultures were grown under two CO₂ concentrations, 450 (control) and 1100 (simulated OA) μatm, and physiological parameters [growth, pigments, catalase (CAT), glutathione reductase (GR), and superoxide dismutase (SOD) activity], as well as transcriptomes (obtained via RNA-seq), were compared. Chlorophyll a (Chl a) and carotenoid (Caro) contents, as well as CAT and GR activities, were significantly increased under OA conditions. Transcriptomic analysis revealed 2,490 differentially expressed unigenes in response to OA, which comprised 1.54% of all unigenes. A total of 1,121 unigenes were upregulated, and 1,369 unigenes were downregulated in OA compared to control conditions. The downregulated expression of bicarbonate transporter and carbonic anhydrase genes was a landmark of OA acclimation. Key genes involved in energy metabolism, e.g., photosynthesis, tricarboxylic acid cycle, oxidative phosphorylation, and nitrogen metabolism, were highly upregulated under OA, contributing to increases in the Chl a (55.05%) and Caro (28.37%). The enhanced antioxidant enzyme activities (i.e. CAT, GR) and upregulated genes (i.e. glutathione peroxidase, ascorbate peroxidase, heat shock protein, 20S proteasome, aldehyde dehydrogenase, and apolipoprotein) benefit cells against the potential lower pH stress condition under OA. In addition, the downregulation of four genes associated with motility suggested that the preserved energy could further boost growth. In conclusion, the present study suggests that K. mikimotoi exhibits efficient gene expression regulation for the utilization of energy and resistance to OA-induced stress. Taken together, K. mikimotoi appeared as a tolerant species in response to OA. Thus, more extensive algal blooms that threaten marine organisms are likely in the future. These findings expand current knowledge on the gene expression of HAB-forming species in response to future OA.