Morphology vs. toxicity: How temperature reshapes Microcystis’ adaptive strategies in a warming world?

Global warming and eutrophication have synergistically intensified cyanobacterial blooms, with Microcystis posing significant ecological and health risks due to microcystin (MC) production. This study investigated how temperature gradients (10 °C, 25 °C, 35 °C, 40 °C) modulate physiological, morphological, and molecular adaptive strategies in M. aeruginosa, focusing on metabolic trade-offs between morphological plasticity and toxin production. Our results demonstrated that robust growth at 35 °C but photosynthetic inhibition at extremes (10 °C/40 °C). High-temperature stress (40 °C) triggered a 101 % increase in MC hypersecretion concurrent with 68 % cell diameter enlargement and 44 % colony fragmentation, comparable to the 25 °C control. In contrast, low-temperature stress (10 °C) promoted intracellular MC retention and a 135 % increase in external layer proportion. Multi-omics analyses demonstrated suppressed carbon fixation, nitrogen metabolism and glycolysis under stress, with compensatory activation of the tricarboxylic acid cycle, the pentose phosphate pathway (NADPH production) and glutathione metabolism for oxidative stress mitigation. Strikingly, MC transporter gene mcyH was pronounced upregulated at 40 °C, and the accompanying polysaccharide synthesis/output (PSO) gene expression strongly correlating with extracellular MC levels, suggesting MC-mediated polysaccharide secretion for environmental adaptation. However, cold-induced external layer formation occurred independently of MC regulatory pathways. Integrative analysis revealed a metabolic trade-off with distinct thermal strategies: high-temperature stress favored MC export, colony downsizing and cellular enlargement, whereas low temperature prioritized intracellular MC storage coupled with antioxidant system activation. These findings elucidate Microcystis’ metabolic trade-offs under thermal stress, highlighting climate-driven bloom persistence mechanisms through synergistic morphological and toxicological adjustments. This study provides critical insights into cyanobacterial dominance mechanisms in warming aquatic ecosystems.