Cryptic arsenic cycling controls oxygenic photosynthesis in Precambrian-analog microbial mats

The delayed rise of atmospheric oxygen, despite the early evolution of oxygenic photosynthesis (OP), remains a central puzzle in Earth history. Numerous ecological and geochemical constraints on OP have been proposed, but the role of environmental stressors at the physiological and ecosystem level is poorly understood. Here we show that Chl-f-harboring cyanobacteria in a high-altitude Andean microbial mat – an analog for Precambrian ecosystems – switch from OP to arsenite-driven anoxygenic photosynthesis (AP) under high light. Using microsensor profiling, mat incubations, and metatranscriptomics, we show that this shift is triggered by the accumulation of reactive oxygen species (ROS), especially hydrogen peroxide, which suppresses OP. Instead of ceasing activity, cyanobacteria reroute electron flow, using arsenite as the electron donor to sustain photosynthesis while avoiding both intracellular ROS from OP and extracellular ROS from aerobic arsenite oxidation. This switch is reversible and coordinated with diel cycles of light and arsenic speciation, sustained by a cryptic arsenic redox cycle, continuously regenerating arsenite for AP. Although the enzymatic basis remains unresolved, these findings reveal a hidden layer of metabolic plasticity in cyanobacteria and suggest that oxidative stress-responsive metabolic shifts may have supported early phototroph survival while limiting oxygen release – potentially contributing to Earth's protracted oxygenation.