Regulatory role of microcystin in the response of microcystin-producing cyanobacteria to elevated CO2: Insights from metabolic profiling

Abstract

The regulatory role of microcystin in the response of microcystin-producing cyanobacteria to elevated CO₂ remains poorly understood. To address this gap, this study compared the responses of wild-type toxic Microcystis PCC 7806 and its mcyB-knockout mutant to elevated CO₂ using metabolomic profiling under nitrogen (N)-rich and N-poor conditions. Under N-poor conditions, elevated CO₂ promoted carbohydrate synthesis and tricarboxylic acid cycle in both strains, without affecting their growth. Under N-rich conditions, both strains exhibited increased biomass with rising CO₂ levels, attributed to enhanced carbohydrate synthesis, tricarboxylic acid cycle, glutamate-glutamine cycle, purine synthesis, and arginine synthesis. However, compared to the mutant, the proliferation of wild-type toxic Microcystis was less stimulated by elevated CO_2. The difference was associated with its reduced activity in the pentose phosphate pathway, likely linked to microcystin synthesis. Besides, the difference was related to higher utilization of glutamate, arginine, and aspartate due to increased microcystin production, indicating the regulatory role of microcystin in the response of microcystin-producing cyanobacteria to elevated CO₂. Importantly, elevated CO₂ could enhance microcystin synthesis by promoting the production of carbon backbones (malonyl CoA), amino acids (including arginine, glutamate and aspartate) and methyl donors (S-adenosylmethionine) of the wild-type toxic Microcystis PCC 7806. Notably, sufficient nitrogen sources were required for increased amino acid and methyl donors synthesis at high CO₂ concentration. The discovery revealed underlying mechanisms behind the potential for elevated CO₂ levels to increase toxicity risk associated with Microcystis blooms.