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Microbial diversity and sulfur cycling in an early earth analogue: from ancient novelty to modern commonality

Hahn, Cassidy Ryan
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Abstract

Life emerged and diversified in the absence of molecular oxygen. The prevailing anoxia and unique sulfur chemistry in the Paleo-, Meso- and Neoarchean, and early Proterozoic eons may have supported microbial communities that differ from those currently thriving on the earth's surface. 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 oxygen intrusion during the NeoProterozoic. We document a remarkably diverse microbial community in the anoxic spring sediments, with 340/516 (65.89%) of genomes recovered in a metagenomic survey belonging to 200 bacterial and archaeal families that were either previously undescribed or that exhibit an extremely rare distribution on the current earth. Such diversity is underpinned by the widespread occurrence of sulfite-, thiosulfate, tetrathionate-, and sulfur-reduction, and paucity of sulfate-reduction machineries in these taxa; hence greatly expanding lineages mediating reductive sulfur cycling processes in the tree of life. Analysis of the overlaying oxygenated water community demonstrated the development of a significantly less diverse community dominated by well-characterized lineages and a 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 in an anoxic earth, but have failed to adapt to earth's progressive oxygenation. Life on earth evolved in an anoxic setting, however, the identity and fate of microorganisms that thrived in a pre-oxygenated earth is poorly understood. Collectively, such patterns strongly suggest that microbial diversity and sulfur cycling processes in a pre-oxygenated earth were drastically different from the currently observed patterns, and that the Great Oxygenation Event has precipitated the near extinction of a wide range of oxygen-sensitive lineages and significantly altered the microbial reductive sulfur-cycling community on earth.

Date
2022-05
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