Significance Cyanobacteria were the first organisms to develop oxygenic photosynthesis using water as a source of electrons. Today they remain widespread primary photosynthetic producers and hold a high biotechnological potential. In cyanobacteria, respiration and photosynthesis are interconnected in a complex network of electron fluxes. The study of cyanobacterial physiology is hampered by the lack of techniques, allowing a direct measurement of the transmembrane electric field that develops across their photosynthetic/respiratory membranes. Here, we characterized a probe of the transmembrane electric field, based on the ElectroChromic Shifts of carotenoids, thus opening unprecedented avenues to bioenergetics studies of these major photosynthetic organisms.