The Oman Drilling Project established an "Active Alteration" multi-borehole observatory in peridotites undergoing low-temperature serpentinization in the Samail Ophiolite. The highly serpentinized rocks are in contact with strongly reducing fluids. Distinct hydrological regimes, governed by differences in rock porosity and fracture density, give rise to steep redox (Eh +200 to −750 mV) and pH (pH range 8.5-11.2) gradients within the 300-400 m deep boreholes. The serpentinites and fluids host an active subsurface ecosystem. Microbial cell abundances in serpentinite vary at least six orders of magnitude, from ≤3.5 × 10 1 to 2.9 × 10 7 cells/g. Low levels of biological sulfate reduction (2-1,000 fmol/ cm 3 /day) can be detected in rock cores, particularly in rocks in contact with reduced groundwaters with pH < 10.5. Thermodesulfovibrio is the predominant sulfate reducer identified via metagenomic sequencing of adjacent groundwater communities. We infer that transport and reaction of microbially generated sulfide with the serpentine and brucite assemblages gives rise to optical darkening and sulfide overprinting, including the formation of tochilinite-vallerite group minerals, potentially serving as an indicator that this system is inhabited by microbial life. Olivine mesh-cores replaced with ferroan brucite and minor awaruite, abundant veins containing hydroandradite garnet and polyhedral serpentine, and late-stage carbonate veins are suggested as targets for future spatially resolved life-detection investigations. The high-quality whole-round core samples that have been preserved can be further probed to define how life distributes itself and functions within a system where chemical disequilibria are sustained by lowtemperature water/rock interaction, and how biosignatures of in situ microbial activity are generated.Plain Language Summary Ultramafic rocks undergoing water/rock interaction, and storing fluids that are far from chemical equilibrium, may be one of the most common habitats in our solar system. Through the Oman Drilling Project we collected >1 km of intact serpentinite in contact with groundwaters. These cores capture parts of the rock-hosted biosphere and show how cells are distributed within serpentinites that vary in their mineralogical, physical and chemical properties. The cores are also biologically active, enabling us to detect specific metabolisms, such as when microorganisms combine hydrogen as reductant and sulfate as an oxidant to fuel their metabolism. Although the distribution of microbial cells in the rock cores is very heterogeneous, there are many intervals where the abundance of cells constitutes robust biomass. In the deeper cores, slow, albeit detectable, microbial sulfate reduction proceeds. We suggest that this pervasive biological activity releases byproducts such as sulfide that can react with the serpentinite and change the optical and chemical properties of the rocks. The feedbacks between the rock alteration and microbial activity produce markers that enable us to focus our sea...
Archaeal methanogens, methanotrophs, and alkanotrophs have a high demand for iron (Fe) and sulfur (S); however, little is known of how they acquire, traffic, deploy, and store these elements. Here, we examined the distribution of homologs of proteins mediating key steps in Fe/S metabolism in model microorganisms, including iron(II) sensing/uptake (FeoAB), sulfide extraction from cysteine (SufS), the biosynthesis of iron-sulfur [Fe-S] clusters (SufBCDE), siroheme (Pch2-dehydrogenase), protoheme (AhbABCD), and cytochrome c (CcmCF), and iron-storage/detoxification (Bfr, FtrA, IssA), among 326 publicly available, complete or metagenome-assembled genomes of archaeal methanogens/methanotrophs/alkanotrophs. Results indicate several prevalent but non-universal features including FeoB, SufBC, and the biosynthetic apparatus for the basic tetrapyrrole scaffold as well as its siroheme (and F 430 ) derivatives. However, several early diverging genomes lacked SufS and pathways to synthesize and deploy heme. Genomes encoding complete versus incomplete heme biosynthetic pathways exhibited an equivalent prevalence of [Fe-S]-cluster binding proteins, suggesting an expansion of catalytic capabilities rather than substitution of heme for [Fe-S] in the former group. Several strains with heme binding proteins lacked heme biosynthesis capabilities while other strains with siroheme biosynthesis capability lacked homologs of known siroheme binding proteins, indicating heme auxotrophy and unknown siroheme biochemistry, respectively. While ferritin proteins involved in ferric oxide storage were widespread, those involved in storing Fe as thioferrate were unevenly distributed. Collectively, the results suggest that differences in the mechanisms of Fe and S acquisition, deployment, and storage have accompanied the diversification of methanogens/methanotrophs/alkanotrophs, possibly in response to differential availability of these elements as these organisms evolved. IMPORTANCE Archaeal methanogens, methanotrophs, and alkanotrophs, argued to be among the most ancient forms of life, have a high demand for iron (Fe) and sulfur (S) for co-factor biosynthesis, among other uses. Here, using comparative bioinformatic approaches applied to 326 genomes, we show that major differences in Fe/S acquisition, trafficking, deployment, and storage exist in this group. Variation in these characters was generally congruent with the phylogenetic placement of these genomes, indicating that variation in Fe/S usage and deployment has contributed to the diversification and ecology of these organisms. However, incongruency was observed among the distribution of cofactor biosynthesis pathways and known protein destinations for those co-factors, suggesting auxotrophy or yet to be discovered pathways for cofactor biosynthesis.
Microbial mat communities are associated with extensive (∼700 km2) and morphologically variable carbonate structures, termed microbialites, in the hypersaline Great Salt Lake (GSL), Utah. However, whether the composition of GSL mat communities covaries with microbialite morphology and lake environment is unknown. Moreover, the potential adaptations that allow the establishment of these extensive mat communities at high salinity (14% to 17% total salts) are poorly understood. To address these questions, microbial mats were sampled from seven locations in the south arm of GSL representing different lake environments and microbialite morphologies. Despite the morphological differences, microbialite-associated mats were taxonomically similar and were dominated by the cyanobacterium Euhalothece and several heterotrophic bacteria. Metagenomic sequencing of a representative mat revealed Euhalothece and subdominant Thiohalocapsa populations that harbor the Calvin cycle and nitrogenase, suggesting they supply fixed carbon and nitrogen to heterotrophic bacteria. Fifteen of the next sixteen most abundant taxa are inferred to be aerobic heterotrophs and, surprisingly, harbor reaction center, rhodopsin, and/or bacteriochlorophyll biosynthesis proteins, suggesting aerobic photoheterotrophic (APH) capabilities. Importantly, proteins involved in APH are enriched in the GSL community relative to that in microbialite mat communities from lower salinity environments. These findings indicate that the ability to integrate light into energy metabolism is a key adaptation allowing for robust mat development in the hypersaline GSL. IMPORTANCE The earliest evidence of life on Earth is from organosedimentary structures, termed microbialites, preserved in 3.481-billion-year-old (Ga) rocks. Phototrophic microbial mats form in association with an ∼700-km2 expanse of morphologically diverse microbialites in the hypersaline Great Salt Lake (GSL), Utah. Here, we show taxonomically similar microbial mat communities are associated with morphologically diverse microbialites across the lake. Metagenomic sequencing reveals an abundance and diversity of autotrophic and heterotrophic taxa capable of harvesting light energy to drive metabolism. The unexpected abundance of and diversity in the mechanisms of harvesting light energy observed in GSL mat populations likely function to minimize niche overlap among coinhabiting taxa, provide a mechanism(s) to increase energy yield and osmotic balance during salt stress, and enhance fitness. Together, these physiological benefits promote the formation of robust mats that, in turn, influence the formation of morphologically diverse microbialite structures that can be imprinted in the rock record.
Little is known of how the confluence of subsurface and surface processes influences the assembly and habitability of hydrothermal ecosystems. To address this knowledge gap, the geochemical and microbial composition of a high temperature, circumneutral hot spring in Yellowstone National Park was examined to identify the sources of solutes and their effect on the ecology of microbial inhabitants. Metagenomic analysis showed populations comprising planktonic and sediment communities are archaeal dominated, are dependent on chemical energy (chemosynthetic), share little overlap in their taxonomic composition, and are differentiated by their inferred use of/tolerance to oxygen and mode of carbon metabolism. The planktonic community is dominated by putative aerobic/aerotolerant autotrophs while the taxonomic composition of the sediment community is more evenly distributed and comprised of anaerobic heterotrophs. These observations are interpreted to reflect sourcing of the spring by anoxic, organic carbon-limited subsurface hydrothermal fluids and ingassing of atmospheric oxygen that selects for aerobic/aerotolerant organisms that have autotrophic capabilities in the water column. Autotrophy and consumption of oxygen by the planktonic community may influence the assembly of the anaerobic and heterotrophic sediment community. Support for this inference comes from higher estimated rates of genome replication in planktonic populations than sediment populations, indicating faster growth in planktonic populations. Collectively, these observations provide new insight into how mixing of subsurface waters and atmospheric oxygen create dichotomy in the ecology of hot spring communities and suggest that planktonic and sediment communities may have been less differentiated taxonomically and functionally prior to the rise of oxygen ∼2.4 Gya. IMPORTANCE Understanding the source and availability of energy capable of supporting life in hydrothermal environments is central to predicting the ecology of microbial life on early Earth when volcanic activity was more widespread. Little is known of the substrates supporting microbial life in circumneutral to alkaline springs, despite their relevance to early Earth habitats. Using metagenomic and informatics approaches, water column and sediment habitats in a representative circumneutral hot spring in Yellowstone were shown to be dichotomous, with the former largely hosting aerobic/aerotolerant autotrophs and the latter primarily hosting anaerobic heterotrophs. This dichotomy is attributed to influx of atmospheric oxygen into anoxic deep hydrothermal spring waters. These results indicate that the ecology of microorganisms in circumneutral to alkaline springs sourced by deep hydrothermal fluids was different prior to the rise of atmospheric oxygen ∼ 2.4 Gya, with planktonic and sediment communities likely to be less differentiated than contemporary circumneutral hot springs.
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