Synechococcus sp. PCC 7002 Performs Anoxygenic Photosynthesis and Deploys Divergent Strategies to Cope with H2Sn and H2O2

Oxygenic and anoxygenic photosynthesis have long been considered defining traits of cyanobacteria. However, whether the important cyanobacterial genus Synechococcus is capable of anoxygenic photosynthesis remains unconfirmed. Here, we report that Synechococcus sp. PCC 7002 is capable of anoxygenic photosynthesis when sulfide (H2S) is supplied as the sole electron donor. Combining the targeted deletion of the sulfide: quinone oxidoreductase gene (Δsqr) with 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) mediated the inhibition of photosystem II. We demonstrated that SQR-mediated H2S oxidation sustains light-dependent CO2 fixation in the absence of O2 evolution. Our genome-wide transcriptomic profiling further revealed that polysulfide (H2Sn) and hydrogen peroxide (H2O2) function as distinct signaling molecules in oxygenic and anoxygenic photosynthesis, modulating central carbon and energy metabolism. In central carbon metabolism, H2Sn markedly upregulates the expression of key genes, including psbA, petC, rbcL, and rbcS, whereas H2O2 downregulates these genes. Within energy metabolism, both molecules converge on oxidative phosphorylation by upregulating genes encoding NADH dehydrogenase and ATP synthase. Furthermore, H2Sₙ treatment uniquely induces sulfur-assimilation and ROS-detoxifying enzymes, conferring a markedly higher tolerance than H2O2. These findings provide direct evidence of anoxygenic photosynthesis in the genus Synechococcus and uncover a dual regulatory network that allows Synechococcus sp. PCC 7002 to balance redox homeostasis under fluctuating oxic/anoxic conditions.