Multiomics Approach Reveals the Inhibitory Effects of Protocatechuic Acid on the Marine Dinoflagellate Scrippsiella...

Harmful algal blooms have occurred more frequently in recent decades and threaten aquaculture, tourism and human health. As a promising control method, most studies on allelopathic mechanisms have focused on the physiological effects on harmful algae. This study employed a multiomics approach to investigate the allelopathic response of the dinoflagellate Scrippsiella acuminata to the allelochemical protocatechuic acid, a phenolic compound known for its inhibitory effects on algal growth. Using transcriptomic, proteomic, and metabolomic analyses, we identified significant changes in gene expression (5247 upregulated and 81 downregulated), protein expression (56 upregulated and 49 downregulated), and metabolite profiles (320 upregulated and 168 downregulated) in response to allelochemical stress. Transcriptomic data revealed an upregulation of genes associated with antioxidant systems and energy metabolism, suggesting a potential antioxidant response to protocatechuic acid exposure. Proteomic analysis highlighted the impact on photosynthesis, energy metabolism, and genetic information processing, with a particular emphasis on the modulation of lipid and carbohydrate metabolism to adapt to stress. Metabolomic profiling corroborated these findings, demonstrating shifts in lipid and amino acid metabolism indicative of an adaptive strategy for energy storage and maintenance of cellular homeostasis under allelochemical stress. Notably, alterations in photosynthesis-related proteins and metabolites indicated a direct effect of protocatechuic acid on the photosynthetic machinery, potentially impairing algal growth and energy production. In conclusion, our multiomics analysis provides a comprehensive view of the complex response of S. acuminata to allelochemical stress, revealing the intricate interplay among genetic, proteomic, and metabolic adjustments. These insights contribute to the understanding of allelopathic interactions and offer potential avenues for the development of novel strategies to manage harmful algal blooms.