More Like this

1. Microbial Diversity and Sulfur Cycling in an Early Earth Analogue: From Ancient Novelty to Modern Commonality

   https://doi.org/10.1128/mbio.00016-22  

   Hahn, C. Ryan ; Farag, Ibrahim F. ; Murphy, Chelsea L. ; Podar, Mircea ; Elshahed, Mostafa S. ; Youssef, Noha H. ( April 2022 , mBio)

   Sousa, Filipa L. ; Schleper, Christa M. (Ed.)

   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 eras 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 eras namely, from the anoxic, surficial light-exposed sediments simulating a preoxygenated earth to overlaid water column where air exposure simulates oxygen intrusion during the Neoproterozoic era. 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 the paucity of sulfate reduction machineries in these taxa. Hence, these processes greatly expand lineages mediating reductive sulfur-cycling processes in the tree of life. An 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 a 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 that once thrived in an anoxic earth but have failed to adapt to earth’s progressive oxygenation. IMPORTANCE Life on earth evolved in an anoxic setting; however, the identity and fate of microorganisms that thrived in a preoxygenated earth are poorly understood. In Zodletone spring, the prevailing geochemical conditions are remarkably similar to conditions prevailing in surficial earth prior to oxygen buildup in the atmosphere. We identify hundreds of previously unknown microbial lineages in the spring and demonstrate that these lineages possess the metabolic machinery to mediate a wide range of reductive sulfur processes, with the capacity to respire sulfite, thiosulfate, sulfur, and tetrathionate, rather than sulfate, which is a reflection of the differences in sulfur-cycling chemistry in ancient versus modern times. Collectively, such patterns strongly suggest that microbial diversity and sulfur-cycling processes in a preoxygenated 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. 

   more » « less
2. Structure of the respiratory MBS complex reveals iron-sulfur cluster catalyzed sulfane sulfur reduction in ancient life

   https://doi.org/10.1038/s41467-020-19697-7  

   Yu, Hongjun ; Haja, Dominik K. ; Schut, Gerrit J. ; Wu, Chang-Hao ; Meng, Xing ; Zhao, Gongpu ; Li, Huilin ; Adams, Michael W. ( December 2020 , Nature Communications)

   Abstract Modern day aerobic respiration in mitochondria involving complex I converts redox energy into chemical energy and likely evolved from a simple anaerobic system now represented by hydrogen gas-evolving hydrogenase (MBH) where protons are the terminal electron acceptor. Here we present the cryo-EM structure of an early ancestor in the evolution of complex I, the elemental sulfur (S 0 )-reducing reductase MBS. Three highly conserved protein loops linking cytoplasmic and membrane domains enable scalable energy conversion in all three complexes. MBS contains two proton pumps compared to one in MBH and likely conserves twice the energy. The structure also reveals evolutionary adaptations of MBH that enabled S 0 reduction by MBS catalyzed by a site-differentiated iron-sulfur cluster without participation of protons or amino acid residues. This is the simplest mechanism proposed for reduction of inorganic or organic disulfides. It is of fundamental significance in the iron and sulfur-rich volcanic environments of early earth and possibly the origin of life. MBS provides a new perspective on the evolution of modern-day respiratory complexes and of catalysis by biological iron-sulfur clusters. 

   more » « less
3. Early planetesimal differentiation and late accretion shaped Earth’s nitrogen budget

   https://doi.org/10.1038/s41467-024-48500-0  

   Wang, Wenzhong ; Walter, Michael J. ; Brodholt, John P. ; Huang, Shichun ( May 2024 , Nature Communications)

   The relative roles of protoplanetary differentiation versus late accretion in establishing Earth’s life-essential volatile element inventory are being hotly debated. To address this issue, we employ first-principles calculations to investigate nitrogen (N) isotope fractionation during Earth’s accretion and differentiation. We find that segregation of an iron core would enrich heavy N isotopes in the residual silicate, while evaporation within a H₂-dominated nebular gas produces an enrichment of light N isotope in the planetesimals. The combined effect of early planetesimal evaporation followed by core formation enriches the bulk silicate Earth in light N isotopes. If Earth is comprised primarily of enstatite-chondrite-like material, as indicated by other isotope systems, then late accretion of carbonaceous-chondrite-like material must contribute ~ 30–100% of the N budget in present-day bulk silicate Earth. However, mass balance using N isotope constraints shows that the late veneer contributes only a limited amount of other volatile elements (e.g., H, S, and C) to Earth.

    

   more » « less
4. Complex Microbial Communities Drive Iron and Sulfur Cycling in Arctic Fjord Sediments

   https://doi.org/10.1128/AEM.00949-19  

   Buongiorno, J. ; Herbert, L. C. ; Wehrmann, L. M. ; Michaud, A. B. ; Laufer, K. ; Røy, H. ; Jørgensen, B. B. ; Szynkiewicz, A. ; Faiia, A. ; Yeager, K. M. ; et al ( July 2019 , Applied and Environmental Microbiology)

   Liu, Shuang-Jiang (Ed.)

   ABSTRACT Glacial retreat is changing biogeochemical cycling in the Arctic, where glacial runoff contributes iron for oceanic shelf primary production. We hypothesize that in Svalbard fjords, microbes catalyze intense iron and sulfur cycling in low-organic-matter sediments. This is because low organic matter limits sulfide generation, allowing iron mobility to the water column instead of precipitation as iron monosulfides. In this study, we tested this with high-depth-resolution 16S rRNA gene libraries in the upper 20 cm at two sites in Van Keulenfjorden, Svalbard. At the site closer to the glaciers, iron-reducing Desulfuromonadales , iron-oxidizing Gallionella and Mariprofundus , and sulfur-oxidizing Thiotrichales and Epsilonproteobacteria were abundant above a 12-cm depth. Below this depth, the relative abundances of sequences for sulfate-reducing Desulfobacteraceae and Desulfobulbaceae increased. At the outer station, the switch from iron-cycling clades to sulfate reducers occurred at shallower depths (∼5 cm), corresponding to higher sulfate reduction rates. Relatively labile organic matter (shown by δ 13 C and C/N ratios) was more abundant at this outer site, and ordination analysis suggested that this affected microbial community structure in surface sediments. Network analysis revealed more correlations between predicted iron- and sulfur-cycling taxa and with uncultured clades proximal to the glacier. Together, these results suggest that complex microbial communities catalyze redox cycling of iron and sulfur, especially closer to the glacier, where sulfate reduction is limited due to low availability of organic matter. Diminished sulfate reduction in upper sediments enables iron to flux into the overlying water, where it may be transported to the shelf. IMPORTANCE Glacial runoff is a key source of iron for primary production in the Arctic. In the fjords of the Svalbard archipelago, glacial retreat is predicted to stimulate phytoplankton blooms that were previously restricted to outer margins. Decreased sediment delivery and enhanced primary production have been hypothesized to alter sediment biogeochemistry, wherein any free reduced iron that could potentially be delivered to the shelf will instead become buried with sulfide generated through microbial sulfate reduction. We support this hypothesis with sequencing data that showed increases in the relative abundance of sulfate reducing taxa and sulfate reduction rates with increasing distance from the glaciers in Van Keulenfjorden, Svalbard. Community structure was driven by organic geochemistry, suggesting that enhanced input of organic material will stimulate sulfate reduction in interior fjord sediments as glaciers continue to recede. 

   more » « less
5. Sulfur cycling likely obscures dynamic biologically‐driven iron redox cycling in contemporary methane seep environments

   https://doi.org/10.1111/1758-2229.13263  

   Baker, Isabel_R ; Girguis, Peter_R ( May 2024 , Environmental Microbiology Reports)

   Deep‐sea methane seeps are amongst the most biologically productive environments on Earth and are often characterised by stable, low oxygen concentrations and microbial communities that couple the anaerobic oxidation of methane to sulfate reduction or iron reduction in the underlying sediment. At these sites, ferrous iron (Fe²⁺) can be produced by organoclastic iron reduction, methanotrophic‐coupled iron reduction, or through the abiotic reduction by sulfide produced by the abundant sulfate‐reducing bacteria at these sites. The prevalence of Fe²⁺in the anoxic sediments, as well as the availability of oxygen in the overlying water, suggests that seeps could also harbour communities of iron‐oxidising microbes. However, it is unclear to what extent Fe²⁺remains bioavailable and in solution given that the abiotic reaction between sulfide and ferrous iron is often assumed to scavenge all ferrous iron as insoluble iron sulfides and pyrite. Accordingly, we searched the sea floor at methane seeps along the Cascadia Margin for microaerobic, neutrophilic iron‐oxidising bacteria, operating under the reasoning that if iron‐oxidising bacteria could be isolated from these environments, it could indicate that porewater Fe²⁺can persist is long enough for biology to outcompete pyritisation. We found that the presence of sulfate in our enrichment media muted any obvious microbially‐driven iron oxidation with most iron being precipitated as iron sulfides. Transfer of enrichment cultures to sulfate‐depleted media led to dynamic iron redox cycling relative to abiotic controls and sulfate‐containing cultures, and demonstrated the capacity for biogenic iron (oxyhydr)oxides from a methane seep‐derived community. 16S rRNA analyses revealed that removing sulfate drastically reduced the diversity of enrichment cultures and caused a general shift from a Gammaproteobacteria‐domainated ecosystem to one dominated byRhodobacteraceae(Alphaproteobacteria). Our data suggest that, in most cases, sulfur cycling may restrict the biological “ferrous wheel” in contemporary environments through a combination of the sulfur‐adapted sediment‐dwelling ecosystems and the abiotic reactions they influence.

    

   more » « less