Abiotic synthesis of amino acids in the recesses of the oceanic lithosphere.

Abiotic hydrocarbons and carboxylic acids are known to be formed on Earth, notably during the hydrothermal alteration of mantle rocks. Although the abiotic formation of amino acids has been predicted both from experimental studies and thermodynamic calculations, its occurrence has not been demonstrated in terrestrial settings. Here, using a multimodal approach that combines high-resolution imaging techniques, we obtain evidence for the occurrence of aromatic amino acids formed abiotically and subsequently preserved at depth beneath the Atlantis Massif (Mid-Atlantic Ridge). These aromatic amino acids may have been formed through Friedel-Crafts reactions catalysed by an iron-rich saponite clay during a late alteration stage of the massif serpentinites. Demonstrating the potential of fluid-rock interactions in the oceanic lithosphere to generate amino acids abiotically gives credence to the hydrothermal theory for the origin of life, and may shed light on ancient metabolisms and the functioning of the present-day deep biosphere.

The rocky road to organics needs drying.

How simple abiotic organic compounds evolve toward more complex molecules of potentially prebiotic importance remains a missing key to establish where life possibly emerged. The limited variety of abiotic organics, their low concentrations and the possible pathways identified so far in hydrothermal fluids have long hampered a unifying theory of a hydrothermal origin for the emergence of life on Earth. Here we present an alternative road to abiotic organic synthesis and diversification in hydrothermal environments, which involves magmatic degassing and water-consuming mineral reactions occurring in mineral microcavities. This combination gathers key gases (N2, H2, CH4, CH3SH) and various polyaromatic materials associated with nanodiamonds and mineral products of olivine hydration (serpentinization). This endogenous assemblage results from re-speciation and drying of cooling C-O-S-H-N fluids entrapped below 600 °C-2 kbars in rocks forming the present-day oceanic lithosphere. Serpentinization dries out the system toward macromolecular carbon condensation, while olivine pods keep ingredients trapped until they are remobilized for further reactions at shallower levels. Results greatly extend our understanding of the forms of abiotic organic carbon available in hydrothermal environments and open new pathways for organic synthesis encompassing the role of minerals and drying. Such processes are expected in other planetary bodies wherever olivine-rich magmatic systems get cooled down and hydrated.

High-pressure synthesis and storage of solid organic compounds in active subduction zones.

Recent thermodynamic and experimental studies have suggested that volatile organic compounds (e.g., methane, formate, and acetate) can be produced and stabilized in subduction zones, potentially playing an important role in the deep carbon cycle. However, field evidence for the high-pressure production and storage of solid organic compounds is missing. Here, we examine forearc serpentinite clasts recovered by drilling mud volcanoes above the Mariana subduction zone. Notable correlations between carbon and iron stable-isotope signatures and fluid-mobile element (B, As and Sb) concentrations provide evidence for the percolation of slab-derived CO2-rich aqueous fluids through the forearc mantle. The presence of carbonaceous matter rich in aliphatic moieties within high-temperature clasts (>350°C) demonstrates that molecular hydrogen production associated with forearc serpentinization is an efficient mechanism for the reduction and conversion of slab-derived CO2-rich fluids into solid organic compounds. These findings emphasize the need to consider the forearc mantle as an important reservoir of organic carbon on Earth.

An Alternative Approach for Assessing Biogenicity.

The search for signs of life in the ancient rock record, extreme terrestrial environments, and other planetary bodies requires a well-established, universal, and unambiguous test of biogenicity. This is notably true for cellular remnants of microbial life, since their relatively simple morphologies resemble various abiogenic microstructures that occur in nature. Although lists of qualitative biogenicity criteria have been devised, debates regarding the biogenicity of many ancient microfossils persist to this day. We propose here an alternative quantitative approach for assessing the biogenicity of putative microfossils. In this theoretical approach, different hypotheses-involving biology or not and depending on the geologic setting-are put forward to explain the observed objects. These hypotheses correspond to specific types of microstructures/systems. Using test samples, the morphology and/or chemistry of these systems are then characterized at the scale of populations. Morphologic parameters include, for example, circularity, aspect ratio, and solidity, while chemical parameters could include elementary ratios (e.g., N/C ratio), isotopic enrichments (e.g., δ13C), or chirality (e.g., molar proportion of stereoisomers), among others. Statistic trends distinguishing the different systems are then searched for empirically. The trends found are translated into "decision spaces" where the different systems are quantitatively discriminated and where the potential microfossil population can be located as a single point. This approach, which is formulated here on a theoretical level, will solve several problems associated with the classical qualitative criteria of biogenicity. Most importantly, it could be applied to reveal the existence of cellular life on other planets, for which characteristics of morphology and chemical composition are difficult to predict.

Tracking hidden organic carbon in rocks using chemometrics and hyperspectral imaging.

Finding traces of life or organic components of prebiotic interest in the rock record is an appealing goal for numerous fields in Earth and space sciences. However, this is often hampered by the scarceness and highly heterogeneous distribution of organic compounds within rocks. We assess here an innovative analytical strategy combining Synchrotron radiation-based Fourier-Transform Infrared microspectroscopy (S-FTIR) and multivariate analysis techniques to track and characterize organic compounds at the pore level in complex oceanic rocks. S-FTIR hyperspectral images are analysed individually or as multiple image combinations (multiset analysis) using Principal Component Analyses (PCA) and Multivariate Curve Resolution - Alternating Least Squares (MCR-ALS). This approach allows extracting simultaneously pure organic and mineral spectral signatures and determining their spatial distributions and relationships. MCR-ALS analysis provides resolved S-FTIR signatures of 8 pure mineral and organic components showing the close association at a micrometric scale of organic compounds and secondary clays formed during rock alteration and known to catalyse organic synthesis. These results highlights the potential of the serpentinizing oceanic lithosphere to generate and preserve organic compounds of abiotic origin, in favour of the hydrothermal theory for the origin of life.

Abiotic formation of condensed carbonaceous matter in the hydrating oceanic crust.

Thermodynamic modeling has recently suggested that condensed carbonaceous matter should be the dominant product of abiotic organic synthesis during serpentinization, although it has not yet been described in natural serpentinites. Here we report evidence for three distinct types of abiotic condensed carbonaceous matter in paragenetic equilibrium with low-temperature mineralogical assemblages hosted by magma-impregnated, mantle-derived, serpentinites of the Ligurian Tethyan ophiolite. The first type coats hydroandraditic garnets in bastitized pyroxenes and bears mainly aliphatic chains. The second type forms small aggregates (~2 µm) associated with the alteration rims of spinel and plagioclase. The third type appears as large aggregates (~100-200 µm), bearing aromatic carbon and short aliphatic chains associated with saponite and hematite assemblage after plagioclase. These assemblages result from successive alteration at decreasing temperature and increasing oxygen fugacity. They affect a hybrid mafic-ultramafic paragenesis commonly occurring in the lower oceanic crust, pointing to ubiquity of the highlighted process during serpentinization.

Characterization of Pustular Mats and Related Rivularia-Rich Laminations in Oncoids From the Laguna Negra Lake (Argentina).

Stromatolites are organo-sedimentary structures that represent some of the oldest records of the early biosphere on Earth. Cyanobacteria are considered as a main component of the microbial mats that are supposed to produce stromatolite-like structures. Understanding the role of cyanobacteria and associated microorganisms on the mineralization processes is critical to better understand what can be preserved in the laminated structure of stromatolites. Laguna Negra (Catamarca, Argentina), a high-altitude hypersaline lake where stromatolites are currently formed, is considered as an analog environment of early Earth. This study aimed at characterizing carbonate precipitation within microbial mats and associated oncoids in Laguna Negra. In particular, we focused on carbonated black pustular mats. By combining Confocal Laser Scanning Microscopy, Scanning Electron Microscopy, Laser Microdissection and Whole Genome Amplification, Cloning and Sanger sequencing, and Focused Ion Beam milling for Transmission Electron Microscopy, we showed that carbonate precipitation did not directly initiate on the sheaths of cyanobacterial Rivularia, which dominate in the mat. It occurred via organo-mineralization processes within a large EPS matrix excreted by the diverse microbial consortium associated with Rivularia where diatoms and anoxygenic phototrophic bacteria were particularly abundant. By structuring a large microbial consortium, Rivularia should then favor the formation of organic-rich laminations of carbonates that can be preserved in stromatolites. By using Fourier Transform Infrared spectroscopy and Synchrotron-based deep UV fluorescence imaging, we compared laminations rich in structures resembling Rivularia to putatively chemically-precipitated laminations in oncoids associated with the mats. We showed that they presented a different mineralogy jointly with a higher content in organic remnants, hence providing some criteria of biogenicity to be searched for in the fossil record.

Mineralizing Filamentous Bacteria from the Prony Bay Hydrothermal Field Give New Insights into the Functioning of Serpentinization-Based Subseafloor Ecosystems.

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.

Microbial diversity in a submarine carbonate edifice from the serpentinizing hydrothermal system of the Prony Bay (New Caledonia) over a 6-year period.

Active carbonate chimneys from the shallow marine serpentinizing Prony Hydrothermal Field were sampled 3 times over a 6 years period at site ST09. Archaeal and bacterial communities composition was investigated using PCR-based methods (clone libraries, Denaturating Gel Gradient Electrophoresis, quantitative PCR) targeting 16S rRNA genes, methyl coenzyme M reductase A and dissimilatory sulfite reductase subunit B genes. Methanosarcinales (Euryarchaeota) and Thaumarchaea were the main archaeal members. The Methanosarcinales, also observed by epifluorescent microscopy and FISH, consisted of two phylotypes that were previously solely detected in two other serpentinitzing ecosystems (The Cedars and Lost City Hydrothermal Field). Surprisingly, members of the hyperthermophilic order Thermococcales were also found which may indicate the presence of a hot subsurface biosphere. The bacterial community mainly consisted of Firmicutes, Chloroflexi, Alpha-, Gamma-, Beta-, and Delta-proteobacteria and of the candidate division NPL-UPA2. Members of these taxa were consistently found each year and may therefore represent a stable core of the indigenous bacterial community of the PHF chimneys. Firmicutes isolates representing new bacterial taxa were obtained by cultivation under anaerobic conditions. Our study revealed diverse microbial communities in PHF ST09 related to methane and sulfur compounds that share common populations with other terrestrial or submarine serpentinizing ecosystems.

Spatial distribution of microbial communities in the shallow submarine alkaline hydrothermal field of the Prony Bay, New Caledonia.

The shallow submarine hydrothermal field of the Prony Bay (New Caledonia) discharges hydrogen- and methane-rich fluids with low salinity, temperature (< 40°C) and high pH (11) produced by the serpentinization reactions of the ultramafic basement into the lagoon seawater. They are responsible for the formation of carbonate chimneys at the lagoon seafloor. Capillary electrophoresis single-strand conformation polymorphism fingerprinting, quantitative polymerase chain reaction and sequence analysis of 16S rRNA genes revealed changes in microbial community structure, abundance and diversity depending on the location, water depth, and structure of the carbonate chimneys. The low archaeal diversity was dominated by few uncultured Methanosarcinales similar to those found in other serpentinization-driven submarine and subterrestrial ecosystems (e.g. Lost City, The Cedars). The most abundant and diverse bacterial communities were mainly composed of Chloroflexi, Deinococcus-Thermus, Firmicutes and Proteobacteria. Functional gene analysis revealed similar abundance and diversity of both Methanosarcinales methanoarchaea, and Desulfovibrionales and Desulfobacterales sulfate-reducers in the studied sites. Molecular studies suggest that redox reactions involving hydrogen, methane and sulfur compounds (e.g. sulfate) are the energy driving forces of the microbial communities inhabiting the Prony hydrothermal system.