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

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 are drastically different than those currently thriving on the earth 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 the relentless oxygen intrusion during the Neo Proterozoic. 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 water community demonstrated that oxygen intrusion lead to 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 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 progressive oxygenation.

Autotrophic biofilms sustained by deeply-sourced groundwater host diverse CPR bacteria implicated in sulfur and hydrogen metabolism

“…Of particular interest are Candidate Phyla Radiation (CPR) bacteria (also known as Patescibacteria) [25][26][27][28] that can form symbioses with host organisms [29][30][31]. Prior surveys have documented CPR bacteria in sulfur-based communities [25,32,33], yet the nature of CPR-host relationships and the roles of CPR in sulfur-based communities remain under-explored.…”

Top‐down enrichment of oil field microbiomes to limit souring and control oil composition during extraction operations

“…We found that each well had a distinct microbial composition with various sulfur‐reducing (or H 2 S‐producing) bacteria as well as other archaea and bacteria found in previous MEOR studies 17,41 . Common bacteria phyla include Proteobacteria, Bacteroidota, Firmicutes, Synergistota, Spirochaetota, Verrucomicrobiota, Desulfobacterota, and Campilobacterota, of which the latter three are prominent sulfur‐metabolizing bacteria 42–45 . These populations were distinct from others in the literature, 13,37 a finding that is not unexpected given that each community is driven by un environmental conditions such as temperature, salinity, pH, nutrient availability, and oil gravity among other factors 25 .…”

“…17,41 Common bacteria phyla include Proteobacteria, Bacteroidota, Firmicutes, Synergistota, Spirochaetota, Verrucomicrobiota, Desulfobacterota, and Campilobacterota, of which the latter three are prominent sulfur-metabolizing bacteria. [42][43][44][45] These populations were distinct from others in the literature, 13,37 a finding that is not unexpected given that each community is driven by un environmental conditions such as temperature, salinity, pH, nutrient availability, and oil gravity among other factors. 25 However, there is no known correlation between native microbial community and MEOR success.…”