Microbial diversity in an early earth analogue: From ancient novelty to modern commonality

Life emerged and diversified in the absence of molecular oxygen 1. The prevailing anoxia and unique sulfur chemistry in the Paleo-, Meso- and Neoarchean, and early Proterozoic eons may have supported microbial communities that are drastically different than those currently thriving on the earth’s surface 2–4. Zodletone spring in southwestern Oklahoma represents a unique habitat where spatial sampling could substitute for geological eons: from the anoxic, surficial light-exposed sediments simulating a preoxygenated earth, to overlaid water column where air exposure simulates the relentless oxygen intrusion during the Neo-Proterozoic 5. We discovered a remarkably diverse microbial community in the spring sediments, with two thirds (340/516) of the metagenomic assembled genomes belonging to 200 bacterial and archaeal families that were either previously undescribed or are extremely rare elsewhere on earth. Such diversity is underpinned by the widespread occurrence of sulfite-, thiosulfate-, tetrathionate-, and sulfur-reduction, in contrast with a paucity of sulfate-reduction metabolism in those taxa. This greatly expands the diversity of lineages mediating reductive sulfur cycling processes in the tree of life. In the overlaying water community oxygen intrusion leads to the establishment of a significantly less diverse community dominated by well-characterized lineages and the prevalence of oxidative sulfur cycling processes. Such transition from ancient novelty to modern commonality underscores the profound impact of the great oxygenation event on the earth’s surficial anoxic community.. It also suggests that novel and rare lineages encountered in current anaerobic habitats could represent taxa once thriving on the anoxic earth that have failed to adapt to the progressive oxygenation.