Disruption of macrophyte-induced algal defence by a cyanobacterial competitor through metabolic shifts and microbiome dysbiosis

Eutrophication and global warming are intensifying cyanobacterial blooms, complicating macrophyte-based restoration. Submerged macrophytes can suppress cyanobacteria and induce defensive aggregation in green algae, but the effects of toxic cyanobacterial metabolites on macrophyte-alga signaling remain unclear. Here, we used a dialysis-bag co-culture system to test how toxic Microcystis aeruginosa affects interactions between Ceratophyllum demersum and Chlorella vulgaris. We quantified C. vulgaris growth, photosynthetic pigments, oxidative responses, apoptosis, and cell aggregation, and profiled C. demersum metabolites and epiphytic bacterial communities. In the absence of M. aeruginosa, C. demersum inhibited C. vulgaris growth and induced strong cell aggregation, accompanied by elevated reactive oxygen species, peroxidase activity, malondialdehyde accumulation, and clustered apoptotic signals. Metabolomic and microbial analyses indicated enhanced flavonoid and organic acid metabolism and coordinated shifts in epiphytic bacteria, suggesting a plant-microbe feedback that strengthened allelopathic and aggregation-inducing effects. In contrast, diffusible secretions from M. aeruginosa altered the C. demersum metabolic profile toward terpenoid-dominated responses, reshaped the epiphytic microbiome, and weakened metabolite-bacteria correlations. These changes reduced the capacity of C. demersum to induce aggregation in C. vulgaris and modified oxidative and apoptotic responses. The findings suggest that toxic cyanobacteria can interfere with macrophyte-mediated interspecific signaling by reprogramming host metabolism and destabilizing plant-associated microbial networks. Cyanobacterial secondary metabolites and lysis products should therefore be considered when assessing macrophyte-based interactions.