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 <i>Synechococcus</i> is capable of anoxygenic photosynthesis remains unconfirmed. Here, we report that <i>Synechococcus</i> 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 (Δ<i>sqr</i>) 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 (H₂S_n) and hydrogen peroxide (H₂O₂) function as distinct signaling molecules in oxygenic and anoxygenic photosynthesis, modulating central carbon and energy metabolism. In central carbon metabolism, H₂S_n markedly upregulates the expression of key genes, including <i>psbA</i>, <i>petC</i>, <i>rbcL</i>, and <i>rbcS</i>, 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 <i>Synechococcus</i> and uncover a dual regulatory network that allows <i>Synechococcus</i> sp. PCC 7002 to balance redox homeostasis under fluctuating oxic/anoxic conditions.