Significance Carbon fixation is arguably one of the most important metabolic processes on Earth. Stand-alone CP12 proteins are major players in the regulation of this pathway in all oxygenic photosynthetic organisms, yet their intrinsic disorder has so far hampered the capturing of a principal part of their structure. Here we provide structural insights into CP12 by investigating an uncharacterized CP12 fusion protein, CBS–CP12, which is widespread among cyanobacteria, and reveal a unique hexameric structure. Our data further extend the existing knowledge of the regulation of photosynthesis and carbon fixation by the CP12 protein family, suggesting a more versatile role of this protein family in global redox regulation, predominantly in bloom-forming cyanobacteria that pose major threats in lakes and reservoirs.