Sulfate assimilation regulates antioxidant defense response of the cyanobacterium <i>Synechococcus elongatus</i> PCC 7942 to high concentrations of carbon dioxide

The adaptive evolution of cyanobacteria over a prolonged period has allowed them to utilize carbon dioxide (CO₂) at the low concentrations found in the atmosphere (0.04% CO₂) for growth. However, whether the exposure of cyanobacteria to high concentrations of CO₂ results in oxidative stress and the activation of antioxidant defense response remains unknown, albeit fluctuations in other culture conditions have been reported to exert these effects. The current study reveals the physiological regulation of the model cyanobacterium <i>Synechococcus elongatus</i> PCC 7942 upon exposure to 1% CO₂ and the underlying mechanism. Exposure to 1% CO₂ was demonstrated to induce oxidative stress and activate antioxidant defense responses in <i>S. elongatus</i>. Further analysis of variations in metabolism between <i>S. elongatus</i> cells grown at 0.04% CO₂ and exposed to 1% CO₂ revealed that sulfate assimilation was enhanced after the exposure to 1% CO₂. A strain of <i>S. elongatus</i> lacking the gene <i>cysR</i>, encoding a global transcriptional regulator for genes involved in sulfate assimilation, was generated by deleting the gene from the genomic DNA. A comparative analysis of the wild-type and <i>cysR</i>-null strains indicated the regulation of the antioxidant response by sulfate assimilation. In addition, lines of evidence were presented that suggest a role of degradation of phycobilisome in the antioxidant response of <i>S. elongatus</i> under conditions of 1% CO₂ and sulfate limitation. This study sheds light on the <i>in situ</i> effects of high CO₂-induced stress on the ecophysiology of cyanobacteria upon exposure to diverse scenarios from a biotechnological and ecological perspective.IMPORTANCECyanobacteria that grow autotrophically with CO₂ as the sole carbon source can be subject to high-CO₂ stress in a variety of biotechnological and ecological scenarios. However, physiological regulation of cyanobacteria in response to high-CO₂ stress remains elusive. Here, we employed microbial physiological, biochemical, and genetic techniques to reveal the regulatory strategies of cyanobacteria in response to high-CO₂ stress. This study, albeit physiological, provides a biotechnological enterprise for manipulating cyanobacteria as the chassis for CO₂ conversion and sheds light on the <i>in situ</i> ecological effects of high CO₂ on cyanobacteria.