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

The global expansion of Microcystis-dominated cyanobacterial blooms (MCBs) threatens aquatic ecosystems health, where Microcystis population comprises coexisting microcystin (MC)-producing (MC) and MC-free (MC) strains. Luteolin, an allelopathic algicide, has shown potential in inhibiting MCMicrocystis growth and MC-production/-release. This study investigated luteolin's effects on co-cultured MC and MCMicrocystis (i.e. Microcystis population), aiming to compare their sensitivity and elucidate mechanisms via MC-production/-release, proteomics, and metabolomics. Results showed that luteolin inhibited Microcystis population growth by 41.10%-58.37%, with MC strain exhibiting greater sensitivity, as indicated by stronger growth inhibition ratio (30.43%-62.61%) and more severe cellular damage for MC strain. Integrated proteomic and metabolomic analyses further revealed the underlying mechanisms of such sensitivity difference: MCMicrocystis 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, MCMicrocystis 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, luteolin increased MCs synthesis and conversation within co-cultured MCMicrocystis cells, potentially exacerbating eco-risks due to prolonged MC-release. This study clarifies the differential sensitivity of MC and MCMicrocystis to allelopathic algicide and their molecular mechanisms, offering insights for developing targeted management plans, based on each strain's survival strategies, to control MCBs.