LAUSR

Significance The oxygenation of the atmosphere about 2.4 billion years ago remodeled global cycles of toxic, redox-sensitive metal(loids), including that of arsenic, which must have represented a cataclysm in the history of life. Our understanding of biological adaptations surrounding this key transition remains unexplored. By estimating the timing of genetic systems for arsenic detoxification, we reveal an expansion of enzymes and pathways that accompanied adaptations to the biotoxicity of oxidized arsenic species produced by Great Oxidation Event. These include enzymes originated via convergent evolution and pathways that use oxygen for enzymatic catalysis. Our results illustrate how life thrived under the stress of metal(loid) toxicity and provide insights into environmental biogeochemical cycling and microbial evolution. The rise of oxygen on the early Earth about 2.4 billion years ago reorganized the redox cycle of harmful metal(loids), including that of arsenic, which doubtlessly imposed substantial barriers to the physiology and diversification of life. Evaluating the adaptive biological responses to these environmental challenges is inherently difficult because of the paucity of fossil records. Here we applied molecular clock analyses to 13 gene families participating in principal pathways of arsenic resistance and cycling, to explore the nature of early arsenic biogeocycles and decipher feedbacks associated with planetary oxygenation. Our results reveal the advent of nascent arsenic resistance systems under the anoxic environment predating the Great Oxidation Event (GOE), with the primary function of detoxifying reduced arsenic compounds that were abundant in Archean environments. To cope with the increased toxicity of oxidized arsenic species that occurred as oxygen built up in Earth’s atmosphere, we found that parts of preexisting detoxification systems for trivalent arsenicals were merged with newly emerged pathways that originated via convergent evolution. Further expansion of arsenic resistance systems was made feasible by incorporation of oxygen-dependent enzymatic pathways into the detoxification network. These genetic innovations, together with adaptive responses to other redox-sensitive metals, provided organisms with novel mechanisms for adaption to changes in global biogeocycles that emerged as a consequence of the GOE.