The interplay between light, arsenic and H2O2 controls oxygenic photosynthesis in a Precambrian analog cyanobacterial mat.

The regulation of O2 production by cyanobacteria is critical to understanding the coevolution of oxygenic photosynthesis (OP) and Earth's redox landscape. This includes their response to electron donors for competitive anoxygenic photosynthesis, like arsenic. In this work, we assessed the effect of arsenic cycling on photosynthetic activity in a modern cyanobacterial mat thriving beneath an arsenate-rich (~9-10 μM) water column in the high-altitude central Andes, using biogeochemical and omics approaches. Microsensor measurements and hyperspectral imaging revealed two O2- producing cyanobacterial layers. During the afternoon, OP ceased in the lower, Chl fdominated layer. Ex-situ measurements revealed that the combination of high light and arsenic induced a prominent rise in local H2O2 concentration, which then coincided with the interruption of OP. Mat incubations suggested that after OP ceased, cyanobacteria transitioned to As(III)-driven anoxygenic photosynthesis using far-red light. Additional incubations and metatranscriptomics on in-situ samples reveal simultaneous As(V) reduction during the day, at sufficiently high rates to supply electron donors for anoxygenic photosynthesis. This study proposes that As(III) can serve as an alternative electron donor for cyanobacterial photosynthesis. It also reveals the crucial role of arsenic in moderating OP, a consequence of the interaction between arsenic and reactive oxygen species under high irradiance. Given the widespread abundance of arsenic in the Precambrian, we further discuss how this regulatory mechanism could have played an important role in the early evolution of OP.