The aerobic biosphere as an O₂ sink before the Great Oxygenation Event: geobiological feedback to solid Earth and surface oxidation

Abstract Microbial O 2 production via oxygenic photosynthesis was vital in oxygenating the Earth’s surface environment during the Great Oxygenation Event (GOE) ca. 2.5 to 2.3 billion years ago. However, geochemical, paleontological and genomic data suggest the emergence of oxygenic photosynthesis precedes the GOE by at least 500 million years. This demonstrates that the first appearance of microbial O 2 in the environment cannot explain the timing of atmospheric oxygenation. Instead, the GOE was facilitated by Earth’s geodynamic evolution, expanding cyanobacterial habitats and the changing redox state of the mantle, decreasing the abundance of reduced surface rocks, volcanic gases and aqueous solutes. These trends ultimately resulted in magnified O 2 production rates and diminished O 2 consumption rates. Thus, the GOE can be understood as a misbalance between O 2 sources and sinks. One of the most critical O 2 sinks on modern Earth is microbial O 2 consumption via aerobic respiration, and accumulating evidence suggests its emergence well before the GOE. However, the role of aerobic microorganisms as an O 2 sink delaying the GOE remains poorly explored. Here, we review the redox evolution of Earth’s mantle and surface environments, as well as the Archean evolution of aerobic microbial metabolisms. Oxygenic photosynthesis released O 2 to the environment, but the secular oxidation of the solid Earth was critical in allowing O 2 accumulation. Aerobic respiration expanded in response to the GOE, but our survey suggests it could have been a critical O 2 sink even earlier. Hence, aerobic respiration can be seen as geobiological feedback to changes in the Earth system from deep in the mantle up to the surface. However, the timing and rate of O 2 consumption by aerobic respiration before the GOE remain poorly constrained. We conclude by highlighting open questions and future research directions to understand the role of the aerobic O 2 sink in delaying the GOE.