Timing of the Precambrian rise in atmospheric oxygen through molecular evolutionary reconstruction of the cyanobacterial sunscreen scytonemin

Most paleo-environmental models argue that Earth’s atmosphere underwent a change from mildly reducing and anoxic, to its present oxygen-rich character sometime after the evolutionary advent of oxygenic photosynthesis in cyanobacteria in the Great Oxidation Event (GOE), the timing of which remains a matter of contention. Presently favored estimates from the geochemical rock record place the GOE between 2.45-2.22 billion years ago (Ga), while fossil or molecular evidence for oxygenation is of a much later and uncertain date (2.1-1.65 Ga). We estimated that the minimal evolutionary age of scytonemin, an indole-alkaloid used by cyanobacteria as an ultraviolet-A (UVA) sunscreen, is approximately 2.3 ± 0.8 Ga through phylogenetic reconstruction of several genes that encode for proteins involved in the biosynthesis of scytonemin, as calibrated against the cyanobacterial fossil record. Since the biologically useful form of scytonemin requires an oxidizing environment, and UVA radiation is only damaging in the presence of free oxygen, the minimal age of the scytonemin biosynthetic operon places a direct constraint on the minimal age of the GOE. Our findings significantly push back in time the biological evidence, providing genomics-derived support for geochemical constraints of the timing of the GOE