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

Abstract

Microbial O2 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 O2 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 O2 production rates and diminished O2 consumption rates. Thus, the GOE can be understood as a misbalance between O2 sources and sinks. One of the most critical O2 sinks on modern Earth is microbial O2 consumption via aerobic respiration, and accumulating evidence suggests its emergence well before the GOE. However, the role of aerobic microorganisms as an O2 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 releasedO2 to the environment, but the secular oxidation of the solid Earth was critical in allowing O2 accumulation. Aerobic respiration expanded in response to the GOE, but our survey suggests it could have been a critical O2 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 O2 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 O2 sink in delaying the GOE.