With history spanning from the first known fossils and oxygenating the Earth’s atmosphere, to performing 25% of modern annual carbon fixation, the photosynthetic prokaryotes, cyanobacteria, are fundamental to life on Earth. They accomplish this feat of carbon fixation by implementing an efficient CO₂-concentrating mechanism (CCM) featuring proteinaceous bacterial microcompartments called carboxysomes. The CCM drives the formation of a CO₂-rich environment inside carboxysomes where the carbon-fixing machinery, ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and carbonic anhydrase, are housed. The internal environment of carboxysomes is more oxidizing than the surrounding cytosol but the chemical permeability across the protein shell of carboxysomes is largely unknown. In this thesis I utilize a redox-sensitive GFP construct with timelapse fluorescence microscopy to track the redox state of immature and mature carboxysomes under perturbed conditions (high/low [CO₂] and addition of redox agents). These experiments have revealed that the redox state and permeability of carboxysomes are dynamic, responding to environmental changes, and capable of returning to the initial steady-state conditions. This work provides critical understanding of the redox-based mechanisms driving carbon-fixing regulation and robustness under changing environmental state essential for implementation of carboxysomes in biotechnological applications and climate change.