<p>Responsible for fixing 25% of carbon dioxide (CO₂) globally, cyanobacteria use carboxysomes to house their CO₂ fixing machinery. The formation and permeability of the proteinaceous shell of carboxysomes is an area of active study. While necessary in air (0.04% CO₂), the shell is not required when cyanobacteria are in high CO₂ levels representative of early Earth. To understand how the carboxysome shell responds to increased CO₂ conditions, we used a Grx1-roGFP2 redox sensor and single cell timelapse fluorescence microscopy to track subcellular redox states of <i>Synechococcus</i> sp. PCC 7002. Comparing different levels of compartmentalization, we targeted the cytosol, a shell-less carboxysomal assembly intermediate called procarboxysomes, and carboxysomes. Carboxysome redox state was dynamic, and, under 3% CO₂ conditions, procarboxysome-like structures formed which were only partially encapsulated and exposed the carboxysome contents to the cytosol. This work expands the adaptability of carboxysomes to environmental conditions and builds understanding of the selective forces that initially drove carboxysome evolution.</p>