| Summary: | Cyanobacteria can perform both anoxygenic and oxygenic photosynthesis, a characteristic which ensured that these organisms were crucial in the evolution of the early Earth and the biosphere. Reactive oxygen species (ROS) produced in oxygenic photosynthesis and reactive sulfur species (RSS) produced in anoxygenic photosynthesis are closely related to intracellular redox equilibrium. ROS comprise superoxide anion (O<sub>2</sub><sup>●−</sup>), hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), and hydroxyl radicals (<sup>●</sup>OH). RSS comprise H<sub>2</sub>S and sulfane sulfur (persulfide, polysulfide, and S<sub>8</sub>). Although the sensing mechanism for ROS in cyanobacteria has been explored, that of RSS has not been elucidated. Here, we studied the function of the transcriptional repressor PerR in RSS sensing in <i>Synechococcus</i> sp. PCC7002 (PCC7002). PerR was previously reported to sense ROS; however, our results revealed that it also participated in RSS sensing. PerR repressed the expression of <i>prxI</i> and downregulated the tolerance of PCC7002 to polysulfide (H<sub>2</sub>S<sub>n</sub>). The reporter system indicated that PerR sensed H<sub>2</sub>S<sub>n</sub>. Cys<sup>121</sup> of the Cys4:Zn<sup>2+</sup> site, which contains four cysteines (Cys<sup>121</sup>, Cys<sup>124</sup>, Cys<sup>160</sup>, and Cys<sup>163</sup>) bound to one zinc atom, could be modified by H<sub>2</sub>S<sub>n</sub> to Cys<sup>121</sup>-SSH, as a result of which the zinc atom was released from the site. Moreover, Cys<sup>19</sup> could also be modified by polysulfide to Cys<sup>19</sup>-SSH. Thus, our results reveal that PerR, a representative of the Cys<sub>4</sub> zinc finger proteins, senses H<sub>2</sub>S<sub>n</sub>. Our findings provide a new perspective to explore the adaptation strategy of cyanobacteria in Proterozoic and contemporary sulfurization oceans.
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