The Lost City hydrothermal field is a dramatic example of the biological potential of serpentinization. Microbial life is prevalent throughout the Lost City chimneys, powered by the hydrogen gas and ...organic molecules produced by serpentinization and its associated geochemical reactions. Microbial life in the serpentinite subsurface below the Lost City chimneys, however, is unlikely to be as dense or active. The marine serpentinite subsurface poses serious challenges for microbial activity, including low porosities, the combination of stressors of elevated temperature, high pH and a lack of bioavailable ∑CO
. A better understanding of the biological opportunities and challenges in serpentinizing systems would provide important insights into the total habitable volume of Earth's crust and for the potential of the origin and persistence of life in Earth's subsurface environments. Furthermore, the limitations to life in serpentinizing subsurface environments on Earth have significant implications for the habitability of subsurface environments on ocean worlds such as Europa and Enceladus. Here, we review the requirements and limitations of life in serpentinizing systems, informed by our research at the Lost City and the underwater mountain on which it resides, the Atlantis Massif. This article is part of a discussion meeting issue 'Serpentinite in the Earth System'.
All living organisms synthesize phospholipids as the primary constituent of their cell membranes. Enzymatic synthesis of diacylphospholipids requires preexisting membrane-embedded enzymes. This ...limitation has led to models of early life in which the first cells used simpler types of membrane building blocks and has hampered integration of phospholipid synthesis into artificial cells. Here we demonstrate an enzyme-free synthesis of natural diacylphospholipids by transacylation in water, which is enabled by a combination of ion pairing and self-assembly between lysophospholipids and acyl donors. A variety of membrane-forming cellular phospholipids have been obtained in high yields. Membrane formation takes place in water from natural alkaline sources such as soda lakes and hydrothermal oceanic vents. When formed vesicles are transferred to more acidic solutions, electrochemical proton gradients are spontaneously established and maintained. This high-yielding non-enzymatic synthesis of natural phospholipids in water opens up new routes for lipid synthesis in artificial cells and sheds light on the origin and evolution of cellular membranes.
Fluids from the ultramafic-hosted Lost City hydrothermal field were analyzed for total dissolved organic carbon and dissolved organic acids. Formate (36–158
μmol/kg) and acetate (1–35
μmol/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.
The Lost City hydrothermal field on the Mid-Atlantic Ridge supports dense microbial life on the lofty calcium carbonate chimney structures. The vent field is fueled by chemical reactions between the ...ultramafic rock under the chimneys and ambient seawater. These serpentinization reactions provide reducing power (as hydrogen gas) and organic compounds that can serve as microbial food; the most abundant of these are methane and formate. Previous studies have characterized the interior of the chimneys as a single-species biofilm inhabited by the Lost City
, but they also indicated that this methanogen is unable to metabolize formate. The new metagenomic results presented here indicate that carbon cycling in these Lost City chimney biofilms could depend on the metabolism of formate by
populations. Additionally, we present evidence for metabolically diverse, formate-utilizing
populations and new genomic and phylogenetic insights into the unique Lost City
Primitive forms of life may have originated around hydrothermal vents at the bottom of the ancient ocean. The Lost City hydrothermal vent field, fueled by just rock and water, provides an analog for not only primitive ecosystems but also potential extraterrestrial rock-powered ecosystems. The microscopic life covering the towering chimney structures at the Lost City has been previously documented, yet little is known about the carbon cycling in this ecosystem. These results provide a better understanding of how carbon from the deep subsurface can fuel rich microbial ecosystems on the seafloor.
Increasing inputs of organic matter (OM) are driving declining dissolved oxygen (DO) concentrations in coastal ecosystems worldwide. The quantity, source, and composition of OM transported to coastal ...ecosystems via stormwater runoff have been altered by land use changes associated with urbanization and subsequent hydrologic flows that accompany urban stormwater management. To elucidate the role of stormwater in the decline of coastal DO, rain event sampling of biochemical oxygen demand (BOD) in samples collected from the outfall of stormwater ponds and wetlands, as well as samples of largely untreated runoff carried by stormwater ditches, was conducted across a range of urban and suburban development densities. Sampling also included measurements of particulate and dissolved carbon and nitrogen, carbon and nitrogen stable isotopes, and chlorophyll-a. Results suggest stormwater may be a significant source of labile OM to receiving waters, especially during the first flush of runoff, even though BOD concentrations vary both among and within sites in response to rain events. BOD variability was best predicted by particulate OM (POM) and chlorophyll-a, rather than the larger pool of dissolved OM. These findings demonstrate the importance of managing episodic stormwater discharge, especially POM, from urbanized areas to mitigate DO impairment in larger downstream systems.
Carbonate‐brucite chimneys are a characteristic of low‐ to moderate‐temperature, ultramafic‐hosted alkaline hydrothermal systems, such as the Lost City hydrothermal field located on the Atlantis ...Massif at 30°N near the Mid‐Atlantic Ridge. These chimneys form as a result of mixing between warm, serpentinization‐derived vent fluids and cold seawater. Previous work has documented the evolution in mineralogy and geochemistry associated with the aging of the chimneys as hydrothermal activity wanes. However, little is known about spatial heterogeneities within and among actively venting chimneys. New mineralogical and geochemical data (87Sr/86Sr and stable C, O, and clumped isotopes) indicate that the brucite and calcite precipitate at elevated temperatures in vent fluid‐dominated domains in the interior of chimneys. Exterior zones dominated by seawater are brucite‐poor and aragonite is the main carbonate mineral. Carbonates record mostly out of equilibrium oxygen and clumped isotope signatures due to rapid precipitation upon vent fluid‐seawater mixing. On the other hand, the carbonates precipitate closer to carbon isotope equilibrium, with dissolved inorganic carbon in seawater as the dominant carbon source and have δ13C values within the range of marine carbonates. Our data suggest that calcite is a primary mineral in the active hydrothermal chimneys and does not exclusively form as a replacement of aragonite during later alteration with seawater. Elevated formation temperatures and lower 87Sr/86Sr relative to aragonite in the same sample suggest that calcite may be the first carbonate mineral to precipitate.
Plain Language Summary
At the Lost City hydrothermal field, warm alkaline fluids are discharging out of uplifted mantle rocks. When vent fluids mix with seawater at the seafloor, carbonate and brucite minerals form spectacular towers up to 60 m high. Systems like Lost City are important because the reaction between water and rocks provides carbon and energy sources for microbial life. However, we still do not fully understand what controls the mineralogy and geochemistry of the Lost City hydrothermal chimneys. In this paper, we suggest that the extent of mixing between the hydrothermal fluids and seawater influences the mineralogy and geochemistry of the chimneys. Calcite, which was previously thought to form only during alteration of aragonite by seawater, can also form during seawater‐hydrothermal fluid mixing. Both calcite and brucite form in the interior of the chimneys where vent fluid is more dominant. Aragonite, on the other hand, forms in the exterior of the structures from seawater‐rich fluids. Lastly, because minerals precipitate rapidly during fluid mixing, the stable isotope geochemistry of the carbonates mostly records the composition and temperature of seawater and not the mixed fluid. Thus, care should be exercised in interpreting mineral geochemical data from similar systems.
Key Points
The mineralogy and geochemistry of Lost City chimneys are controlled by the extent of mixing between hydrothermal fluids and seawater
Brucite and calcite precipitate in vent fluid dominated zones while aragonite forms in the exterior of the structures in seawater‐rich zones
Carbonates precipitate in isotopic disequilibrium and record the O and C stable isotope composition of seawater dissolved inorganic carbon
Although the serpentinite‐hosted Lost City hydrothermal field (LCHF) was discovered more than 20 years ago, it remains unclear whether and how the presence of microbes affects the mineralogy and ...textures of the hydrothermal chimney structures. Most chimneys have flow textures comprised of mineral walls bounding paleo‐channels, which are preserved in inactive vent structures to a varying degree. Brucite lines the internal part of these channels, while aragonite dominates the exterior. Calcite is also present locally, mostly associated with brucite. Based on a combination of microscopic and geochemical analyses, we interpret brucite, calcite, and aragonite as primary minerals that precipitate abiotically from mixing seawater and hydrothermal fluids. We also observed local brucite precipitation on microbial filaments and, in some cases, microbial filaments may affect the growth direction of brucite crystals. Brucite is more fluorescent than carbonate minerals, possibly indicating the presence of organic compounds. Our results point to brucite as an important substrate for microbial life in alkaline hydrothermal systems.
Plain Language Summary
Water‐serpentinite reactions at the Lost City hydrothermal field (LCHF) are considered similar to the interactions between seawater and volcanic rocks of the early Earth. The vent fluids that form as a result of this interaction are rich in organic compounds that serve as food and hydrogen that provides energy for microbial life. Systems such as Lost City are ideal sites for investigating processes relevant to early life on Earth. Dense microbial communities live in the mineral structures that form from mixing between vent fluids and seawater at the LCHF. The effect of these microbial inhabitants on the mineralogy and textures of the hydrothermal chimneys is still unknown. This study aims to better understand the mineralogy of the hydrothermal chimneys at Lost City and the relationships between microbes and minerals. Calcite and brucite form in the interior of the chimneys, while aragonite forms on the exterior. Brucite forms inorganic mineral membranes that bound cavities where microbes may live. Unlike calcite and aragonite, brucite is spatially closely associated with microbial activity.
Key Points
Lost City hydrothermal chimneys preserve flow textures defined by mineral membranes bounding paleo‐channels and form a network of cavities
The backbone of the chimney structure is initially brucite. Carbonates precipitate on brucite as the chimneys continue to form
Brucite is the preferred substrate for the growth of microbial biofilms within the chimneys
IODP Expedition 357 used two seabed drills to core 17 shallow holes at 9 sites across Atlantis Massif ocean core complex (Mid-Atlantic Ridge 30°N). The goals of this expedition were to investigate ...serpentinization processes and microbial activity in the shallow subsurface of highly altered ultramafic and mafic sequences that have been uplifted to the seafloor along a major detachment fault zone. More than 57 m of core were recovered, with borehole penetration ranging from 1.3 to 16.4 meters below seafloor, and core recovery as high as 75% of total penetration in one borehole. The cores show highly heterogeneous rock types and alteration associated with changes in bulk rock chemistry that reflect multiple phases of magmatism, fluid-rock interaction and mass transfer within the detachment fault zone. Recovered ultramafic rocks are dominated by pervasively serpentinized harzburgite with intervals of serpentinized dunite and minor pyroxenite veins; gabbroic rocks occur as melt impregnations and veins. Dolerite intrusions and basaltic rocks represent the latest magmatic activity. The proportion of mafic rocks is volumetrically less than the amount of mafic rocks recovered previously by drilling the central dome of Atlantis Massif at IODP Site U1309. This suggests a different mode of melt accumulation in the mantle peridotites at the ridge-transform intersection and/or a tectonic transposition of rock types within a complex detachment fault zone. The cores revealed a high degree of serpentinization and metasomatic alteration dominated by talc-amphibole-chlorite overprinting. Metasomatism is most prevalent at contacts between ultramafic and mafic domains (gabbroic and/or doleritic intrusions) and points to channeled fluid flow and silica mobility during exhumation along the detachment fault. The presence of the mafic lenses within the serpentinites and their alteration to mechanically weak talc, serpentine and chlorite may also be critical in the development of the detachment fault zone and may aid in continued unroofing of the upper mantle peridotite/gabbro sequences.
New technologies were also developed for the seabed drills to enable biogeochemical and microbiological characterization of the environment. An in situ sensor package and water sampling system recorded real-time variations in dissolved methane, oxygen, pH, oxidation reduction potential (Eh), and temperature and during drilling and sampled bottom water after drilling. Systematic excursions in these parameters together with elevated hydrogen and methane concentrations in post-drilling fluids provide evidence for active serpentinization at all sites. In addition, chemical tracers were delivered into the drilling fluids for contamination testing, and a borehole plug system was successfully deployed at some sites for future fluid sampling. A major achievement of IODP Expedition 357 was to obtain microbiological samples along a west–east profile, which will provide a better understanding of how microbial communities evolve as ultramafic and mafic rocks are altered and emplaced on the seafloor. Strict sampling handling protocols allowed for very low limits of microbial cell detection, and our results show that the Atlantis Massif subsurface contains a relatively low density of microbial life.
•Seabed rock drills and real-time fluid monitoring for first time in ocean drilling•First time recovery of continuous sequences along oceanic detachment fault zone•Highly heterogeneous rock type and alteration in shallow detachment fault zone•High methane and hydrogen concentrations in Atlantis Massif shallow basement•Oceanic serpentinites potentially provide important niches for microbial life
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.
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