Timing the evolution of antioxidant enzymes in cyanobacteria

The ancestors of cyanobacteria generated Earth's first biogenic molecular oxygen, but how they dealt with oxidative stress remains unconstrained. Here we investigate when superoxide dismutase enzymes (SODs) capable of removing superoxide free radicals evolved and estimate when Cyanobacteria originated. Our Bayesian molecular clocks, calibrated with microfossils, predict that stem Cyanobacteria arose 3300-3600 million years ago. Shortly afterwards, we find phylogenetic evidence that ancestral cyanobacteria used SODs with copper and zinc cofactors (CuZnSOD) during the Archaean. By the Paleoproterozoic, they became genetically capable of using iron, nickel, and manganese as cofactors (FeSOD, NiSOD, and MnSOD respectively). The evolution of NiSOD is particularly intriguing because it corresponds with cyanobacteria's invasion of the open ocean. Our analyses of metalloenzymes dealing with reactive oxygen species (ROS) now demonstrate that marine geochemical records alone may not predict patterns of metal usage by phototrophs from freshwater and terrestrial habitats. How early photosynthesizers managed oxidative stress remains relatively unresolved. Analyses of enzymes dealing with reactive oxygen species traces the evolutionary history of superoxide dismutases and finds evidence of CuZnSOD in the ancestor of all cyanobacteria, dating back to the Archaean.

Automated summary

Research shows that ancestral cyanobacteria had the ability to deal with oxidative stress as early as the Archaean, gradually evolving more cofactors. The evolutionary history of metalloenzymes reveals how early cyanobacteria managed reactive oxygen species.