Marine heatwaves intensify competition between toxigenic microalgae and cultured macroalgae

Abstract Harmful algal blooms (HABs) and marine heatwaves (MHWs) are occurring with increasing frequency, posing significant threats to marine ecosystems. Macroalgae cultivation has been demonstrated to inhibit the occurrence of HABs. However, how MHWs affect the interactive dynamics between toxigenic microalgae and cultivated macroalgae remains poorly understood. In this study, an economically-important macroalga Gracilariopsis lemaneiformis and a globally-distributed bloom-forming toxigenic microalga Heterosigma akashiwo were grown in monoculture and coculture systems under a simulated MHW event to bridge this gap. Co-culture with G. lemaneiformis significantly reduced the relative growth rate of H. akashiwo. This inhibitory effect could be attributed to allelochemicals secreted by G. lemaneiformis, which decreased the photosynthetic efficiency (Fv/Fm) of the microalga. Notably, heatwave conditions exacerbated these inhibitory effects, and H. akashiwo showed no signs of recovery even after the post-heatwave recovery period. In the co-culture system, increased microalgal toxicity reduced the phycobiliprotein content in G. lemaneiformis. Despite increased metabolic activity in the macroalga, its overall relative growth rates ultimately decreased, with heatwaves exacerbating this reduction. Metabolomic analysis revealed that both the heatwave and co-cultivation with toxic microalgae significantly disrupted the metabolic homeostasis of G. lemaneiformis, particularly its carbon and nitrogen, lipid, and nucleotide metabolisms, ultimately forcing the macroalgae to reallocate energy resources toward essential survival functions. These findings indicate that MHWs could intensify competition between H. akashiwo and G. lemaneiformis, providing novel insights into the potential ecological risks posed by toxigenic microalgae and MHWs to aquaculture.