Unraveling the effects of allelopathic algicide on Microcystis population: microcystin pollution risk assessment and proteomic-metabolomic insights into the sensitivity of toxic and non-toxic strains

The global expansion of Microcystis -dominated cyanobacterial blooms (MCBs) threatens aquatic ecosystems health, where Microcystis comprises coexisting microcystin (MC)-producing (MC + ) and MC-free (MC – ) strains. Luteolin, an allelopathic algicide, has shown potential in inhibiting MC + Microcystis growth and MC-production/-release. This study investigated luteolin's effects on co-cultured MC + and MC – Microcystis ( Microcystis population), comparing their sensitivity and elucidating mechanisms via MC-production/-release, proteomic, and metabolomic. Results showed that luteolin inhibited Microcystis population growth by 41.10% to 58.37%, with MC + strains exhibiting greater sensitivity, as indicated by stronger growth inhibition ratio (30.43% to 62.61%) and more severe cellular damage. Integrated proteomic and metabolomic analyses further revealed the underlying mechanisms of such sensitivity difference: MC + Microcystis exhibited severe impairments in photosynthetic activity, cell membrane composition, and antioxidant systems, alongside disruptions in protein biosynthesis, nucleotide degradation, and hindered DNA replication and repair. In contrast, MC – Microcystis experienced similar but milder disturbances, while promptly initiating compensatory responses. It enhanced carbohydrate metabolism and ATP synthase activity, promoted DNA replication and protein biosynthesis, and activated inflammatory responses to counteract luteolin stress. Additionally, although luteolin significantly decreased MC levels in the aqueous phase to 14.04   μg/L, it increased MC synthesis and retention within co-cultured MC + Microcystis cells, potentially exacerbating eco-risks due to prolonged MC release. This study clarifies the differential sensitivity of MC + and MC – Microcystis to allelopathic algicides and their molecular mechanisms, offering insights for developing targeted management plans based on each strain's survival strategies to control MCBs.