TESTING THE OXYGEN PARADOX WITH ANTIOXIDANT-DEFICIENT CYANOBACTERIA

The light reactions of oxygenic photosynthesis produce reactive oxygen species (ROS) that can damage cellular components and lead to cell death. Thus, the co-evolution of an antioxidant system was necessary for the survival of photosynthetic organisms. But this presents a potential evolutionary paradox. Which came first: antioxidants or oxygenic photosynthesis? If photosynthesis evolved first, how was the photosynthetic electron transport (PET) system protected against ROS? If antioxidants evolved first, what was the selective pressure for their origin? At least two possibilities exist. 1) Photosynthesis evolved first. Since the primordial environment was anaerobic, oxygen could have diffused out of cells before being converted to ROS. Then the gradual oxygenation of the environment would have selected for the evolution of antioxidant systems. 2) Antioxidant systems evolved first. Non-biological sources of ROS (UV and mineralogical reactions) selected for the evolution of antioxidants before the evolution of oxygenic photosynthesis. The first organisms that possessed antioxidants would have been able to live closer to the water's surface, and would have been pre-adapted for dealing with photosynthetically produced ROS. We tested these hypotheses by growing wild type and mutant cyanobacteria (Synechococcus PCC7942 sodB^-—FeSOD deletion) under primordial atmospheres (2.5%-20% CO₂ in N₂). Preliminary results support scenario #1. When grown in air, the sodB^- strain has a lower growth rate than the wild type. However, when the two strains are grown in 2.5% CO₂ in N₂, there is no difference in the growth rates, indicating that the presence or absence of the iron superoxide dismutase has no effect under these conditions. If scenario #2 was correct, we would have expected to see slower growth rates in the sodB^- strain under both atmospheric conditions. Our results support the hypothesis that oxygenic photosynthesis evolved before antioxidant systems and provided the selection pressure for them. However, since PCC7942 possesses two SODs (FeSOD and MnSOD), we still cannot rule out the second hypothesis, that the antioxidant system was a necessary pre-adaptation for photosynthesis. (This research is supported by a grant from the NASA/Arkansas Space Grant Consortium.)