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Molecular Evidence for an Active Microbial Methane Cycle in Subsurface Serpentinite-Hosted Groundwaters in the Samail Ophiolite, Oman.

ABSTRACT: Serpentinization can generate highly reduced fluids replete with hydrogen (H₂) and methane (CH₄), potent reductants capable of driving microbial methanogenesis and methanotrophy, respectively. However, CH₄ in serpentinized waters is thought to be primarily abiogenic, raising key questions about the relative importance of methanogens and methanotrophs in the production and consumption of CH₄ in these systems. Herein, we apply molecular approaches to examine the functional capability and activity of microbial CH₄ cycling in serpentinization-impacted subsurface waters intersecting multiple rock and water types within the Samail Ophiolite of Oman. Abundant 16S rRNA genes and transcripts affiliated with the methanogenic genus Methanobacterium were recovered from the most alkaline (pH, >10), H₂- and CH₄-rich subsurface waters. Additionally, 16S rRNA genes and transcripts associated with the aerobic methanotrophic genus Methylococcus were detected in wells that spanned varied fluid geochemistry. Metagenomic sequencing yielded genes encoding homologs of proteins involved in the hydrogenotrophic pathway of microbial CH₄ production and in microbial CH₄ oxidation. Transcripts of several key genes encoding methanogenesis/methanotrophy enzymes were identified, predominantly in communities from the most hyperalkaline waters. These results indicate active methanogenic and methanotrophic populations in waters with hyperalkaline pH in the Samail Ophiolite, thereby supporting a role for biological CH₄ cycling in aquifers that undergo low-temperature serpentinization.IMPORTANCE Serpentinization of ultramafic rock can generate conditions favorable for microbial methane (CH₄) cycling, including the abiotic production of hydrogen (H₂) and possibly CH₄ Systems of low-temperature serpentinization are geobiological targets due to their potential to harbor microbial life and ubiquity throughout Earth's history. Biomass in fracture waters collected from the Samail Ophiolite of Oman, a system undergoing modern serpentinization, yielded DNA and RNA signatures indicative of active microbial methanogenesis and methanotrophy. Intriguingly, transcripts for proteins involved in methanogenesis were most abundant in the most highly reacted waters that have hyperalkaline pH and elevated concentrations of H₂ and CH₄ These findings suggest active biological methane cycling in serpentinite-hosted aquifers, even under extreme conditions of high pH and carbon limitation. These observations underscore the potential for microbial activity to influence the isotopic composition of CH₄ in these systems, which is information that could help in identifying biosignatures of microbial activity on other planets.

SUBMITTER: Kraus EA

PROVIDER: S-EPMC7783335 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Microbial abundance and diversity in deep subsurface environments is dependent upon the availability of energy and carbon. However, supplies of oxidants and reductants capable of sustaining life within mafic and ultramafic continental aquifers undergoing low-temperature water-rock reaction are relatively unknown. We conducted an extensive analysis of the geochemistry and microbial communities recovered from fluids sampled from boreholes hosted in peridotite and gabbro in the Tayin block of the Samail Ophiolite in the Sultanate of Oman. The geochemical compositions of subsurface fluids in the ophiolite are highly variable, reflecting differences in host rock composition and the extent of fluid-rock interaction. Principal component analysis of fluid geochemistry and geologic context indicate the presence of at least four fluid types in the Samail Ophiolite ("gabbro," "alkaline peridotite," "hyperalkaline peridotite," and "gabbro/peridotite contact") that vary strongly in pH and the concentrations of H2, CH4, Ca2+, Mg2+, [Formula: see text], [Formula: see text], trace metals, and DIC. Geochemistry of fluids is strongly correlated with microbial community composition; similar microbial assemblages group according to fluid type. Hyperalkaline fluids exhibit low diversity and are dominated by taxa related to the Deinococcus-Thermus genus Meiothermus, candidate phyla OP1, and the family Thermodesulfovibrionaceae. Gabbro- and alkaline peridotite- aquifers harbor more diverse communities and contain abundant microbial taxa affiliated with Nitrospira, Nitrosospharaceae, OP3, Parvarcheota, and OP1 order Acetothermales. Wells that sit at the contact between gabbro and peridotite host microbial communities distinct from all other fluid types, with an enrichment in betaproteobacterial taxa. Together the taxonomic information and geochemical data suggest that several metabolisms may be operative in subsurface fluids, including methanogenesis, acetogenesis, and fermentation, as well as the oxidation of methane, hydrogen and small molecular weight organic acids utilizing nitrate and sulfate as electron acceptors. Dynamic nitrogen cycling may be especially prevalent in gabbro and alkaline peridotite fluids. These data suggest water-rock reaction, as controlled by lithology and hydrogeology, constrains the distribution of life in terrestrial ophiolites.

Project description:The southeastern part of New Caledonia main island (Grande Terre) is the location of a large ophiolitic formation that hosts several hyperalkaline springs discharging high pH (∼11) and warm (<40°C) fluids enriched in methane (CH4) and hydrogen (H2). These waters are produced by the serpentinization of the ultrabasic rock formations. Molecular surveys had previously revealed the prokaryotic diversity of some of these New Caledonian springs, especially from the submarine chimneys of Prony Bay hydrothermal field. Here we investigate the microbial community of hyperalkaline waters from on-land springs and their relationships with elevated concentrations of dissolved H2 (21.1-721.3 μmol/L) and CH4 (153.0-376.6 μmol/L). 16S rRNA gene analyses (metabarcoding and qPCR) provided evidence of abundant and diverse prokaryotic communities inhabiting hyperalkaline fluids at all the collected springs. The abundance of prokaryotes was positively correlated to the H2/CH4 ratio. Prokaryotes consisted mainly of bacteria that use H2 as an energy source, such as microaerophilic Hydrogenophaga/Serpentinimonas (detected in all sources on land) or anaerobic sulfate-reducing Desulfonatronum, which were exclusively found in the most reducing (Eh ref H2 ∼ -700 mV) and the most H2-enriched waters discharging at the intertidal spring of the Bain des Japonais. The relative abundance of a specific group of uncultured Methanosarcinales that thrive in serpentinization-driven ecosystems emitting H2, considered potential H2-consuming methanogens, was positively correlated with CH4 concentrations, and negatively correlated to the relative abundance of methylotrophic Gammaproteobacteria. Firmicutes were also numerous in hyperalkaline waters, and their relative abundance (e.g., Gracilibacter or Dethiobacter) was proportional to the dissolved H2 concentrations, but their role in the H2 budget remains to be assessed. The prokaryotic communities thriving in New Caledonia hyperalkaline waters are similar to those found in other serpentinite-hosted high-pH waters worldwide, such as Lost City (North Atlantic) and The Cedars (California).

Project description:The Atlantis Massif rises 4,000 m above the seafloor near the Mid-Atlantic Ridge and consists of rocks uplifted from Earth's lower crust and upper mantle. Exposure of the mantle rocks to seawater leads to their alteration into serpentinites. These aqueous geochemical reactions, collectively known as the process of serpentinization, are exothermic and are associated with the release of hydrogen gas (H2), methane (CH4), and small organic molecules. The biological consequences of this flux of energy and organic compounds from the Atlantis Massif were explored by International Ocean Discovery Program (IODP) Expedition 357, which used seabed drills to collect continuous sequences of shallow (<16 m below seafloor) marine serpentinites and mafic assemblages. Here, we report the census of microbial diversity in samples of the drill cores, as measured by environmental 16S rRNA gene amplicon sequencing. The problem of contamination of subsurface samples was a primary concern during all stages of this project, starting from the initial study design, continuing to the collection of samples from the seafloor, handling the samples shipboard and in the lab, preparing the samples for DNA extraction, and analyzing the DNA sequence data. To distinguish endemic microbial taxa of serpentinite subsurface rocks from seawater residents and other potential contaminants, the distributions of individual 16S rRNA gene sequences among all samples were evaluated, taking into consideration both presence/absence and relative abundances. Our results highlight a few candidate residents of the shallow serpentinite subsurface, including uncultured representatives of the Thermoplasmata, Acidobacteria, Acidimicrobia, and ChloroflexiIMPORTANCE The International Ocean Discovery Program Expedition 357-"Serpentinization and Life"-utilized seabed drills to collect rocks from the oceanic crust. The recovered rock cores represent the shallow serpentinite subsurface of the Atlantis Massif, where reactions between uplifted mantle rocks and water, collectively known as serpentinization, produce environmental conditions that can stimulate biological activity and are thought to be analogous to environments that were prevalent on the early Earth and perhaps other planets. The methodology and results of this project have implications for life detection experiments, including sample return missions, and provide a window into the diversity of microbial communities inhabiting subseafloor serpentinites.

Project description:Abstract Visible‐shortwave infrared (VSWIR) imaging spectrometers map composition remotely with spatial context, typically at many meters‐scale from orbital and airborne data. Here, we evaluate VSWIR imaging spectroscopy capabilities at centimeters to sub‐millimeter scale at the Samail Ophiolite, Oman, where mafic and ultramafic lithologies and their alteration products, including serpentine and carbonates, are exposed in a semi‐arid environment, analogous to similar mineral associations observed from Mars orbit that will be explored by the Mars‐2020 rover. At outcrop and hand specimen scales, VSWIR spectroscopy (a) identifies cross‐cutting veins of calcite, dolomite, magnesite, serpentine, and chlorite that record pathways and time‐order of multiple alteration events of changing fluid composition; (b) detects small‐scale, partially altered remnant pyroxenes and localized epidote and prehnite that indicate protolith composition and temperatures and pressures of multiple generations of faulting and alteration, respectively; and (c) discriminates between spectrally similar carbonate and serpentine phases and carbonate solid solutions. In natural magnesite veins, minor amounts of ferrous iron can appear similar to olivine's strong 1‐μm absorption, though no olivine is present. We also find that mineral identification for carbonate and serpentine in mixtures with each other is strongly scale‐ and texture‐dependent; ∼40 area% dolomite in mm‐scale veins at one serpentinite outcrop and ∼18 area% serpentine in a calcite‐rich travertine outcrop are not discriminated until spatial scales of <∼1–2 cm/pixel. We found biological materials, for example bacterial mats versus vascular plants, are differentiated using wavelengths <1 μm while shortwave infrared wavelengths >1 μm are required to identify most organic materials and distinguish most mineral phases. Key Points Meso‐to micro‐scale imaging spectroscopy identifies and maps carbonates, serpentine, and other hydrothermal phases in the Oman ophiolite Pigmentation from multiple types of biological materials including mats in travertine springs are distinguished even in shallow waters Detection thresholds of carbonate and serpentine when mixed can be >20area%, which has implications for interpretation of planetary data

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Molecular Evidence for an Active Microbial Methane Cycle in Subsurface Serpentinite-Hosted Groundwaters in the Samail Ophiolite, Oman.

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