Abiotic oxidants promoted cyanobacteria’s evolution and Earth’s oxidation

Abstract

<p>Oxygenic photosynthesis by cyanobacteria, green algae and plants effectively converts solar energy and provides free oxygen, which is vital to life. In Earth’s history, the innovation of oxygenic photosynthesis absolutely is a pivotal event because the released O₂ initiated the redox revolution of the Earth surface system, ultimately leading to the rise of atmospheric oxygen level around 2.4 Ga at the Archean-Proterozoic transition (the Great Oxidation Event, GOE). As we know, cyanobacteria originated from its ancestors, anoxygenic phototrophs, and a basic requirement for the evolution of oxygen-producing photosynthesis is that the early oxygen-producing organisms should not be killed by their metabolic products (e.g., intracellular O₂). That means, prior to the innovation of oxygenic photosynthesis, ancestral cyanobacteria should have gained the ability to cope with the toxicity of O₂ and reactive oxygen species (ROS, e.g., hydroxyl radical (•OH), hydrogen peroxide (H₂O₂)). However, there emerges a chicken-and-egg dilemma that oxygenic photosynthesis and free oxygen, which came first?</p><p>Recent phylogenetic analyses^<a>1</a> indicate that antioxidant enzymes deeply encoded in genome of Archaea and Bacteria, even in the Last Universal Common Ancestor (LUCA). This suggests that early life including ancestral cyanobacteria were accessible to abiotic oxidants, so that they acquired a defensive ability against oxidants even utilized these oxidants. Accordingly, the source of abiotic oxidants on the early Earth is the key to decipher the evolution of oxygenic photosynthesis.</p><p>Here, we introduce the advance in the discovery of Archean abiotic oxygen-producing pathway that involves the generation of H₂O₂ and O₂ at mineral-water interfaces (<a>Figure 1</a>). In the Archean, mineral abrasion in turbulent subaqueous environments could have served as a persistent source of abiotic oxidants, creating an evolutionary impetus for the origin of oxygenic photosynthesis^<a>2</a>.</p>