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Despite their potential importance as analogs of primitive microbial metabolisms, the knowledge of the structure and functioning of the deep ecosystems associated with serpentinizing environments is hampered by the lack of accessibility to relevant systems. These hyperalkaline environments are depleted in dissolved inorganic carbon (DIC), making the carbon sources and assimilation pathways in the associated ecosystems highly enigmatic. The Prony Bay Hydrothermal Field (PHF) is an active serpentinization site where, similar to Lost City (Mid-Atlantic Ridge), high-pH fluids rich in H2 and CH4 are discharged from carbonate chimneys at the seafloor, but in a shallower lagoonal environment. This study aimed to characterize the subsurface microbial ecology of this environment by focusing on the earliest stages of chimney construction, dominated by the discharge of hydrothermal fluids of subseafloor origin. By jointly examining the mineralogy and the microbial diversity of the conduits of juvenile edifices at the micrometric scale, we find a central role of uncultivated bacteria belonging to the Firmicutes in the ecology of the PHF. These bacteria, along with members of the phyla Acetothermia and Omnitrophica, are identified as the first chimneys inhabitants before archaeal Methanosarcinales. They are involved in the construction and early consolidation of the carbonate structures via organomineralization processes. Their predominance in the most juvenile and nascent hydrothermal chimneys, and their affiliation with environmental subsurface microorganisms, indicate that they are likely discharged with hydrothermal fluids from the subseafloor. They may thus be representative of endolithic serpentinization-based ecosystems, in an environment where DIC is limited. In contrast, heterotrophic and fermentative microorganisms may consume organic compounds from the abiotic by-products of serpentinization processes and/or from life in the deeper subsurface. We thus propose that the Firmicutes identified at PHF may have a versatile metabolism with the capability to use diverse organic compounds from biological or abiotic origin. From that perspective, this study sheds new light on the structure of deep microbial communities living at the energetic edge in serpentinites and may provide an alternative model of the earliest metabolisms. [ABSTRACT FROM AUTHOR]

Abstract: Active serpentinization systems are abundant on present-day Earth and are of increasing interest because water–rock reactions lead to alkaline, Ca–OH fluids that have the potential to sequester CO2 and form reduced chemical species (e.g. CH4 and H2) that can support chemolithoautotrophy. We present a study of alkaline (pH 10–12) springs in the Voltri Massif (Italy) that focuses on the sources and cycling of inorganic carbon in the basement rocks, the interacting fluids, and the resulting surface carbonate deposits. Most springs are located in mantle rocks that underwent varying degrees of ocean-floor serpentinization and incorporation of carbon (as carbonate and organic carbon) in the Jurassic, which is preserved during subsequent subduction and uplift onto the continent. The springs are fed by meteoric water that evolves into alkaline, Ca-rich spring waters that have 2–3 times higher Ca concentrations than the adjacent rivers. Our study is consistent with previous reaction path modeling and identifies the formation of clay minerals in serpentinites that have been altered by alkaline fluids. These strongly altered basement rocks contain up to 2wt.% C in the shallow subsurface, also documented by the presence of late calcite veins. Concentrations of dissolved inorganic carbon (DIC) of the alkaline fluids are generally low (<16μmol/L) and δ13CDIC is between −24.2‰ and +1.3‰. We argue that the concentrations and isotopic composition of the DIC in the alkaline waters provide evidence for 1) the precipitation of calcium carbonate under closed-system conditions with respect to atmospheric CO2 and 2) removal of DIC by microbial activity in the subsurface. Late-stage uptake of atmospheric CO2 in the shallow subsurface or at the exit sites subsequent to water–rock–microbe interactions in the basement result in fluids with lower pH and Ca, and enrichment in DIC and 13C. At the surface, interaction of the high pH, Ca–OH fluids with atmospheric CO2 causes precipitation of carbonates as travertines or crusts on the basement rocks, storing CO2 as calcium carbonate. Carbonate precipitation at the exit sites is strongly dominated by kinetic processes leading to carbon and oxygen isotope compositions as low as −27.2‰ and −18.7‰, respectively. With increasing distance from the springs, the 13C and 18O content of the carbonate increases and the fluid pH changes towards neutral. Our study shows that surficial carbonate precipitation plays a subordinate role in carbon sequestration, but that the evolution from Mg–HCO3 spring waters to Ca–OH waters removes significant amounts of carbon, presumably in the subsurface. We calculate that the serpentinites have the capacity to sequester up to 0.50 to 2.05×109 mol carbon per year and conclude that they can take up significantly more CO2 than they currently contain. [Copyright &y& Elsevier]

Abstract: Mantle rocks exposed on the seafloor constitute a highly reactive chemical and thermal system, in which interaction with seawater to produce serpentinite has major consequences for lithospheric cooling, global geochemical cycles, and microbial activity. Serpentinite-hosted hydrothermal activity is exemplified by the Lost City Hydrothermal Field (30°N, Mid-Atlantic Ridge) where fluid–rock reactions in the underlying ultramafic rocks result in high concentrations of abiotic hydrogen, methane, C2 + alkanes, and formate. Such systems have been proposed as possible analogs to the Early Earth environments that gave rise to the first biochemical pathways. Thus, characterizing the local microbial communities and their potential link with abiogenic compounds is of particular significance. Here we demonstrate that in active carbonate chimneys where microbial sulfate reduction is important, up to 50% of the microbial biomass is synthesized from mantle carbon. Conversely, mantle carbon contributes only ∼10% of the biomass in areas with minimal sulfate reduction. We attribute this difference to greater incorporation of formate or methane by the dominant microbial species, the Lost City Methanosarcinales, in locations where sulfate reducers are able to facilitate this assimilation. The ability of autotrophic communities at Lost City to capitalize on the steady stream of chemical products resulting from serpentinization reactions and to utilize abiogenic mantle carbon lend credence to the hypothesis that early biosynthetic pathways could have developed in similar environments. [Copyright &y& Elsevier]

Abstract: Fluids from the ultramafic-hosted Lost City hydrothermal field were analyzed for total dissolved organic carbon and dissolved organic acids. Formate (36–158μmol/kg) and acetate (1–35μmol/kg) concentrations are higher than in other fluids from unsedimented hydrothermal vents, and are a higher ratio of the total dissolved organic carbon than has been found in most marine geothermal systems. Isotopic evidence is consistent with an abiotic formation mechanism for formate, perhaps during serpentinization processes in the sub-surface. Further support comes from previous studies where the abiological formation of low molecular weight organic acids has been shown to be thermodynamically favorable during hydrothermal alteration of olivine, and laboratory studies in which the reduction of carbon dioxide to formate has been confirmed. As the second most prevalent carbon species after methane, formate may be an important substrate to microbial communities in an environment where dissolved inorganic carbon is limited. Acetate is found in locations where sulfate reduction is believed to be important and is likely to be a microbial by-product, formed either directly by autotrophic metabolic activity or indirectly during the fermentative degradation of larger organic molecules. Given the common occurrence of exposed ultramafic rocks and active serpentinization within the worlds ocean basins, the abiotic formation of formate may be an important process supporting life in these high pH environments and may have critical implications to understanding the organic precursors from which life evolved. [Copyright &y& Elsevier]

International Ocean Discovery Program Expedition 357 drilled 17 boreholes across the Atlantis Massif with the goals of investigating carbon cycling and the presence of life in a zone of active serpentinization. The expedition recovered multiple lithologies including gabbros, basalts, carbonate sands, and serpentinites. A subset of contrasting lithologies were analyzed for apolar lipid content to determine if non-volatile organic molecules can be detected in the oceanic subsurface. The definitive detection and identification of abiotic and biological lipids in the subsurface of an actively serpentinizing system would be a significant step towards understanding a variety of scientific processes, including the evolution of pre-biotic chemistry, microbial habitability, and the global carbon cycle. Given the high potential for contamination during drilling, a suite of materials used in sample collection and processing were also analyzed to characterize their signatures. An n-alkane series ranging from C 18 to C 30 with δ 13 C isotopic values of −30.9‰ to −28.8‰ was present in lithologically diverse samples. Multiple lines of evidence point to the rock saw used to remove core exteriors during sample processing as the source of these compounds. Many of the other sample-handling procedures designed to reduce surface contamination were determined to be effective and could be implemented in future projects. This result highlights the value of careful prevention and characterization of contamination to allow for more accurate interpretations of complex and dynamic subsurface processes, and the importance that future reports of these compounds occurs in conjunction with thorough contamination assessments. [ABSTRACT FROM AUTHOR]