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 CO2. 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.