Microaerobic steroid biosynthesis and the molecular fossil record of Archean life

Abstract

The power of molecular oxygen to drive many crucial biogeochemical processes, from cellular respiration to rock weathering, makes reconstructing the history of its production and accumulation a first-order question for understanding Earth’s evolution. Among the various geochemical proxies for the presence of O2 in the environment, molecular fossils offer a unique record of O2 where it was first produced and consumed by biology: in sunlit aquatic habitats. As steroid biosynthesis requires molecular oxygen, fossil steranes have been used to draw inferences about aerobiosis in the early Precambrian. However, better quantitative constraints on the O2 requirement of this biochemistry would clarify the implications of these molecular fossils for environmental conditions at the time of their production. Here we demonstrate that steroid biosynthesis is a microaerobic process, enabled by dissolved O2 concentrations in the nanomolar range. We present evidence that microaerobic marine environments (where steroid biosynthesis was possible) could have been widespread and persistent for long periods of time prior to the earliest geologic and isotopic evidence for atmospheric O2. In the late Archean, molecular oxygen likely cycled as a biogenic trace gas, much as compounds such as dimethylsulfide do today.