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Cyanobacterial mats were hotspots of biogeochemical cycling during the Precambrian. However, mechanisms that controlled O₂ release by these ecosystems are poorly understood. In an analog to Proterozoic coastal ecosystems, the Frasassi sulfidic springs mats, we studied the regulation of oxygenic and sulfide-driven anoxygenic photosynthesis (OP and AP) in versatile cyanobacteria, and interactions with sulfur reducing bacteria (SRB). Using microsensors and stable isotope probing we found that dissolved organic carbon (DOC) released by OP fuels sulfide production, likely by a specialized SRB population. Increased sulfide fluxes were only stimulated after the cyanobacteria switched from AP to OP. O₂ production triggered migration of large sulfur-oxidizing bacteria from the surface to underneath the cyanobacterial layer. The resultant sulfide shield tempered AP and allowed OP to occur for a longer …