Organic Biosignature Degradation in Hydrothermal and Serpentinizing Environments: Implications for Life Detection on Icy Moons and Mars.

Evidence of liquid water is a primary indicator of habitability on the icy moons in our outer solar system as well as on terrestrial planets such as Mars. If liquid water-containing environments host life, some of its organic remains can be fossilized and preserved as organic biosignatures. However, inorganic materials may also be present and water-assisted organic-inorganic reactions can transform the organic architecture of biological remains. Our understanding of the fate of these organic remains can be assisted by experimental simulations that monitor the chemical changes that occur in microbial organic matter due to the presence of water and minerals. We performed hydrothermal experiments at temperatures between 100°C and 300°C involving lipid-rich microbes and natural serpentinite mineral mixtures generated by the subaqueous hydrothermal alteration of ultramafic rock. The products reveal what the signals of life may look like when subjected to water-organic-inorganic reactions. Straight- and branched-chain lipids in unaltered samples are joined by cyclization and aromatization products in hydrothermally altered samples. Hydrothermal reactions produce distinct products that are not present in the starting materials, including small, single-ring, heteroatomic, and aromatic compounds such as indoles and phenols. Hydrothermal reactions in the presence of serpentinite minerals lead to significant reduction of these organic structures and their replacement by diketopiperazines (DKPs) and dihydropyrazines (DHPs), which may be compounds that are distinct to organic-inorganic reactions. Given that the precursors of DKPs and DHPs are normally lost during early diagenesis, the presence of these compounds can be an indicator of coexisting recent life and hydrothermal processing in the presence of minerals. However, laboratory experiments reveal that the formation and preservation of these compounds can only occur within a distinct temperature window. Our findings are relevant to life detection missions that aim to access hydrothermal and serpentinizing environments in the subsurfaces of icy moons and Mars.

Quantifying Preservation Potential: Lipid Degradation in a Mars-Analog Circumneutral Iron Deposit.

Comparisons between the preservation potential of Mars-analog environments have historically been qualitative rather than quantitative. Recently, however, laboratory-based artificial maturation combined with kinetic modeling techniques have emerged as a potential means by which the preservation potential of solvent-soluble organic matter can be quantified in various Mars-analog environments. These methods consider how elevated temperatures, pressures, and organic-inorganic interactions influence the degradation of organic biomarkers post-burial. We used these techniques to investigate the preservation potential of deposits from a circumneutral iron-rich groundwater system. These deposits are composed of ferrihydrite (Fe5HO8 · 4H2O), an amorphous iron hydroxide mineral that is a common constituent of rocks found in ancient lacustrine environments on Mars, such as those observed in Gale Crater. Both natural and synthetic ferrihydrite samples were subjected to hydrous pyrolysis to observe the effects of long-term burial on the mineralogy and organic content of the samples. Our experiments revealed that organic-inorganic interactions in the samples are dominated by the transformation of iron minerals. As amorphous ferrihydrite transforms into more crystalline species, the decrease in surface area results in the desorption of organic matter, potentially rendering them more susceptible to degradation. We also find that circumneutral iron-rich deposits provide unfavorable conditions for the preservation of solvent-soluble organic matter. Quantitative comparisons between preservation potentials as calculated when using kinetic parameters show that circumneutral iron-rich deposits are ∼25 times less likely to preserve solvent-soluble organic matter compared with acidic, iron-rich environments. Our results suggest that circumneutral iron-rich deposits should be deprioritized in favor of acidic iron- and sulfur-rich deposits when searching for evidence of life with solvent extraction techniques.

Artificial Maturation of Iron- and Sulfur-Rich Mars Analogues: Implications for the Diagenetic Stability of Biopolymers and Their Detection with Pyrolysis-Gas Chromatography-Mass Spectrometry.

Acidic iron- and sulfur-rich streams are appropriate analogues for the late Noachian and early Hesperian periods of martian history, when Mars exhibited extensive habitable environments. Any past life on Mars may have left behind diagnostic evidence of life that could be detected at the present day. For effective preservation, these remains must have avoided the harsh radiation flux at the martian surface, survived geological storage for billions of years, and remained detectable within their geochemical environment by analytical instrument suites used on Mars today, such as thermal extraction techniques. We investigated the detectability of organic matter within sulfur stream sediments that had been subjected to artificial maturation by hydrous pyrolysis. After maturation, the samples were analyzed by pyrolysis-gas chromatography-mass spectrometry (py-GC-MS) to determine whether organic matter could be detected with this commonly used technique. We find that macromolecular organic matter can survive the artificial maturation process in the presence of iron- and sulfur-rich minerals but cannot be unambiguously distinguished from abiotic organic matter. However, if jarosite and goethite are present in the sulfur stream environment, they interfere with the py-GC-MS detection of organic compounds in these samples. Clay reduces the obfuscating effect of the oxidizing minerals by providing nondeleterious adsorption sites. We also find that after a simple alkali and acid leaching process that removes oxidizing minerals such as iron sulfates, oxides, and oxyhydroxides, the sulfur stream samples exhibit much greater organic responses during py-GC-MS in terms of both abundance and diversity of organic compounds, such as the detection of hopanes in all leached samples. Our results suggest that insoluble organic matter can be preserved over billions of years of geological storage while still retaining diagnostic organic information, but sample selection strategies must either avoid jarosite- and goethite-rich outcrops or conduct preparative chemistry steps to remove these oxidants prior to analysis by thermal extraction techniques.

Pyrolysis of Carboxylic Acids in the Presence of Iron Oxides: Implications for Life Detection on Missions to Mars.

The search for, and characterization of, organic matter on Mars is central to efforts in identifying habitable environments and detecting evidence of life in the martian surface and near surface. Iron oxides are ubiquitous in the martian regolith and are known to be associated with the deposition and preservation of organic matter in certain terrestrial environments, thus iron oxide-rich sediments are potential targets for life-detection missions. The most frequently used protocol for martian organic matter characterization (also planned for use on ExoMars) has been thermal extraction for the transfer of organic matter to gas chromatography-mass spectrometry (GC-MS) detectors. For the effective use of thermal extraction for martian samples, it is necessary to explore how potential biomarker organic molecules evolve during this process in the presence of iron oxides. We have thermally decomposed iron oxides simultaneously with (z)-octadec-9-enoic and n-octadecanoic acids and analyzed the products through pyrolysis-GC-MS. We found that the thermally driven dehydration, reduction, and recrystallization of iron oxides transformed fatty acids. Overall detectability of products greatly reduced, molecular diversity decreased, unsaturated products decreased, and aromatization increased. The severity of this effect increased as reduction potential of the iron oxide and inferred free radical formation increased. Of the iron oxides tested hematite showed the least transformative effects, followed by magnetite, goethite, then ferrihydrite. It was possible to identify the saturation state of the parent carboxylic acid at high (0.5 wt %) concentrations by the distribution of n-alkylbenzenes in the pyrolysis products. When selecting life-detection targets on Mars, localities where hematite is the dominant iron oxide could be targeted preferentially, otherwise thermal analysis of carboxylic acids, or similar biomarker molecules, will lead to enhanced polymerization, aromatization, and breakdown, which will in turn reduce the fidelity of the original biomarker, similar to changes normally observed during thermal maturation.