Regulatory Mechanisms of Microcystis in Response to Stress Following Gradual Transitions to Cold Temperatures

Overwintering cells play a crucial role in Microcystis blooms; however, the mechanisms underlying this process are not yet fully understood. In this study, we investigated the response mechanism of Microcystis aeruginosa to a gradual temperature decline (GTD) by simulating temperature shifts from autumn to winter. Here, the difference of the growth, cell viability, chlorophyll fluorescence, and oxidative stress between GTD group and direct low‐temperature treatment (DLT) group were compared. We also determined the trade‐offs between defensive and active strategies for coping with GTD treatment by conducting metabolomics and transcriptomic analysis. Our findings revealed that the growth of M. aeruginosa cells subjected to gradual temperature decline decreased significantly; however, they were able to recover rapidly once normal conditions were restored. Following the gradual decrease in temperature, several genes associated with photosynthesis, carbohydrate metabolism, oxidative phosphorylation and peptidoglycan biosynthesis in M. aeruginosa were downregulated. In contrast, genes involved in microcystin production—specifically, mcyB‐G , mcyI and mcyJ —and those related to the methionine salvage pathway were upregulated compared with those in cells subjected to direct low‐temperature treatment (DLT). Significant enrichment of metabolites such as L‐proline, γ‐aminobutyric acid (GABA), maltitol, nerol and panose was observed in the GTD group compared with the DLT group. This study integrated physiological, metabolite and transcriptomic data to characterise cold‐induced changes in M. aeruginosa . Our findings demonstrate that the energy requirements of M. aeruginosa cells can be reduced by downregulating energy and carbohydrate metabolism. Additionally, M. aeruginosa cells can regulate metabolites, including microcystin and the methionine salvage pathway, to survive cold stress. These results vividly underscore the remarkable physiological plasticity of M. aeruginosa in adapting to incremental environmental alterations. This adaptability not only provides valuable insights into the survival mechanisms of this species but also has significant implications for understanding the ecological dynamics of cyanobacterial blooms in changing environments, providing new insights into the mechanisms underlying seasonal cyanobacterial blooms and the pivotal roles of signalling and microcystin regulation.