The Effect of Oxygen on Biochemical Networks and the Evolution of Complex Life

The evolution of oxygenic photosynthesis and ensuing oxygenation of Earth’s atmosphere represent a major transition in the history of life. Although many organisms retreated to anoxic environments, others evolved to use oxygen as a high-potential redox couple while concomitantly mitigating its toxicity. To understand the changes in biochemistry and enzymology that accompanied adaptation to O2, we integrated network analysis with information on enzyme evolution to infer how oxygen availability changed the architecture of metabolic networks. Our analysis revealed the existence of four discrete groups of networks of increasing complexity, with transitions between groups being contingent on the presence of key metabolites, including molecular oxygen, which was required for transition into the largest networks.