Inferred ancestry of scytonemin biosynthesis proteins in cyanobacteria indicates a response to Paleoproterozoic oxygenation

Abstract

Protection from radiation damage is an important adaptation for phototrophic microbes. Living in surface, shallow water, and peritidal environments, cyanobacteria are especially exposed to long-wavelength ultraviolet (UVA) radiation. Several groups of cyanobacteria within these environments are protected from UVA damage by the production of the pigment scytonemin. Paleontological evidence of cyanobacteria in UVA-exposed environments from the Proterozoic, and possibly as early as the Archaean, suggests a long evolutionary history of radiation protection within this group. We show that phylogenetic analyses of enzymes in the scytonemin biosynthesis pathway support this hypothesis and reveal a deep history of vertical inheritance of this pathway within extant cyanobacterial diversity. Referencing this phylogeny to cyanobacterial molecular clocks suggests that scytonemin production likely appeared during the early Proterozoic, soon after the Great Oxygenation Event. This timing is consistent with an adaptive scenario for the evolution of scytonemin production, wherein the threat of UVA-generated reactive oxygen species becomes significantly greater once molecular oxygen is more pervasive across photosynthetic environments.