Life on Mars: chemical arguments and clues from Martian meteorites

Primitive terrestrial life – defined as a chemical system able to transfer its molecular information via self-replication and to evolve – probably originated from the evolution of reduced organic molecules in liquid water. Several sources have been proposed for the prebiotic organic molecules: terrestrial primitive atmosphere (methane or carbon dioxide), deep-sea hydrothermal systems, and extraterrestrial meteoritic and cometary dust grains. The study of carbonaceous chondrites, which contain up to 5% by weight of organic matter, has allowed close examination of the delivery of extraterrestrial organic material. Eight proteinaceous amino acids have been identified in the Murchison meteorite among more than 70 amino acids. Engel reported that l-alanine was surprisingly more abundant than d-alanine in the Murchison meteorite. Cronin also found excesses of l-enantiomers for nonprotein amino acids. A large collection of micrometeorites has been recently extracted from Antarctic old blue ice. In the 50- to 100-μm size range, carbonaceous micrometeorites represent 80% of the samples and contain 2% of carbon, on average. They might have brought more carbon than that involved in the present surficial biomass. The early histories of Mars and Earth clearly show similarities. Liquid water was once stable on the surface of Mars, attesting the presence of an atmosphere capable of deccelerating C-rich micrometeorites. Therefore, primitive life may have developed on Mars as well and fossilized microorganisms may still be present in the near subsurface. The Viking missions to Mars in 1976 did not find evidence of either contemporary or past life, but the mass spectrometer on the lander aeroshell determined the atmospheric composition, which has allowed a family of meteorites to be identified as Martian. Although these samples are essentially volcanic in origin, it has been recognized that some of them contain carbonate inclusions and even veins that have a carbon isotopic composition indicative of an origin from Martian atmospheric carbon dioxide. The oxygen isotopic composition of these carbonate deposits allows calculation of the temperature regime existing during formation from a fluid that dissolved the carbon dioxide. As the composition of the fluid is unknown, only a temperature range can be estimated, but this falls between 0° and 90°C, which would seem entirely appropriate for life processes. It was such carbonate veins that were found to host putative microfossils. Irrespective of the existence of features that could be considered to be fossils, carbonate-rich portions of Martian meteorites tend to have material, at more than 1000 ppm, that combusts at a low temperature; i.e., it is an organic form of carbon. Unfortunately, this organic matter does not have a diagnostic isotopic signature so it cannot be unambiguously said to be indigenous to the samples. However, many circumstantial arguments can be made to the effect that it is cogenetic with the carbonate and hence Martian. If it could be proved that the organic matter was preterrestrial, then the isotopic fractionation between it and the carbon is in the right sense for a biological origin. Received: January 22, 1998 / Accepted: February 16, 1998     

A Search for Extraterrestrial Amino Acids in Carbonaceous Antarctic Micrometeorites

Antarctic micrometeorites (AMMs) in the 100–400 m size range are the dominant mass fraction of extraterrestrial material accreted by the Earth today. A high performance liquid chromatography (HPLC) based technique exploited at the limits of sensitivity has been used to search for the extraterrestrial amino acids -aminoisobutyric acid (AIB) and isovaline in AMMs. Five samples, each containing about 30 to 35 grains, were analyzed. All the samples possess a terrestrial amino acid component, indicated by the excess of the L-enantiomers of common protein amino acids. In only one sample (A91) was AIB found to be present at a level significantly above the background blanks. The concentration of AIB (280 ppm), and the AIB/isovaline ratio (10), in this sample are both much higher than in CM chondrites. The apparently large variation in the AIB concentrations of the samples suggests that AIB may be concentrated in rare subset of micrometeorites. Because the AIB/isovaline ratio in sample A91 is much larger than in CM chondrites, the synthesis of amino acids in the micrometeorite parent bodies might have involved a different process requiring an HCN-rich environment, such as that found in comets. If the present day characteristics of the meteorite and micrometeorite fluxes can be extrapolated back in time, then the flux of large carbonaceous micrometeorites could have contributed to the inventory of prebiotic molecules on the early Earth.     

D-Amino Acids in Living Higher Organisms

The homochirality of biological amino acids (L-amino acids) andof the RNA/DNA backbone (D-ribose) might have become establishedbefore the origin of life. It has been considered that D-aminoacids and L-sugars were eliminated on the primitive Earth.Therefore, the presence and function of D-amino acids in livingorganisms have not been studied except for D-amino acids in thecell walls of microorganisms. However, D-amino acids wererecently found in various living higher organisms in the form offree amino acids, peptides, and proteins. Free D-aspartate andD-serine are present and may have important physiologicalfunctions in mammals. D-amino acids in peptides are well knownas opioid peptides and neuropeptides. In protein, D-aspartateresidues increase during aging. This review deals with recentadvances in the study of D-amino acids in higher organisms.     

From interstellar amino acids to prebiotic catalytic peptides: a review

Amino acids were most likely available on the primitive Earth, produced in the primitive atmosphere or in hydrothermal vents. Import of extraterrestrial amino acids may have represented the major supply, as suggested by micrometeorite collections and simulation experiments in space and in the laboratory. Selective condensation of amino acids in water has been achieved via N-carboxy anydrides. Homochiral peptides with an alternating sequence of hydrophobic and hydrophilic amino acids adopt stereoselective and thermostable beta-pleated sheet structures. Some of the homochiral beta-sheets strongly accelerate the hydrolysis of oligoribonucleotides. The beta-sheet-forming peptides have also been shown to protect their amino acids from racemization. Even if peptides are not able to self-replicate, i.e., to replicate a complete sequence from the mixture of amino acids, the accumulation of chemically active peptides on the primitive Earth appears plausible via thermostable and stereoselective beta-sheets made of alternating sequences.     

Imitating Prebiotic Homochirality on Earth

We show how the amino acids needed on prebiotic earth in their homochiral L form can be produced by a reaction of L-alpha-methyl amino acids—that have been identified in the Murchison meteorite—with alpha-keto acids under credible prebiotic conditions. When they are simply heated together they perform a process of decarboxylative transamination but with almost no chiral transfer, and that in the wrong direction, producing D-amino acids from the L-alpha-methyl amino acids. With copper ion a square planar complex with two of the reaction intermediates is formed, and now there is the desired L to L transformation, producing small enantioexcesses of the normal L-amino acids. We also show how these can be amplified, not by making more of the L form but by increasing its concentration in water solution. The process can start with a miniscule excess and in one step generate water solutions with L/D ratios in the over 90% region. Kinetic processes can exceed the results from equilibria. We have also examined such amplifications with ribonucleosides, and have shown that initial modest excesses of the D-nucleosides can be amplified to afford water solutions with D to L ratios in the high 90’s. We have shown that the homochiral compound has two effects on the solubility of the racemate. On one hand it decreases the solubility of the racemate by its role in the solubility product, as a theoretical equation predicts. On the other hand, it increases the solubility of the racemate by changing the nature of the solvent, acting as a cosolvent with the water. This explains why the amplification, while large, is not as large as the simple theoretical equation predicts. Thus when credible examples are produced where small enantioexcesses of D-ribose are created under credible prebiotic conditions, the prerequisites for the RNA world will have been exemplified.     

The origin of life on Earth

Terrestrial life can be schematically described as organic molecules organized in liquid water. According to Oparin's hypothesis, organic building blocks required for early life were produced from simple organic molecules formed in a primitive reducing atmosphere. Precursors of lipids, nucleic acids and enzymes obtained in the laboratory under simulating conditions are reviewed. Geochemists favor now a less reducing atmosphere dominated by carbon dioxide. In such an atmosphere, very few building blocks are formed under prebiotic conditions. Import of extraterrestrial organic molecules may represent an alternative supply. Experimental support for such an alternative scenario is examined in comets, cosmic dust, meteorites and micrometeorites. Even the prebiotic broth receives today severe criticism for being implausible. In contrast to the classical scenario, a chemoautotrophic origin of life is discussed. Finally, interesting information related to early terrestrial life may be gained from Mars exploration.     

Lichens, new and promising material from experiments in astrobiology

Many lichen species are regarded as extremophiles in terms of temperature, radiation and desiccation survival. Therefore, lichens have been previously proposed, together with unicellular algae and bacteria, as the living system most likely to resist the extreme conditions of outer space. This enables, following the “Panspermia” theory, speculation about the possibility of life transfer between Earth and other planets. Different experiments have been designed to establish the survival capability of these organisms exposed to space conditions. In particular, the damaging effect of solar UV was studied under various protecting conditions. Different lichen species were exposed to space in the BIOPAN-5 and BIOPAN-6 facilities of the European Space Agency located at the outer shell of the Russian Earth orbiting FOTON M2 satellite. Chlorophyll fluorescence and gas exchange systems were used for the measurement of photosynthetic parameters. All exposed lichens, independently of the filters used, showed after the flight nearly the same photosynthetic activity as measured before the flight. These findings suggest that lichens could stay alive in space even completely exposed to massive UV and cosmic radiation, which have been proved being lethal for bacteria and other microorganisms. Improvements and possible upgrading of the existing experiment designs are also explored in view of a future and more intensive use of lichens in Astrobiology.     

Prebiotic materials from on and off the early Earth

One of the greatest puzzles of all time is how did life arise? It has been universally presumed that life arose in a soup rich in carbon compounds, but from where did these organic molecules come? In this article, I will review proposed terrestrial sources of prebiotic organic molecules, such as Miller-Urey synthesis (including how they would depend on the oxidation state of the atmosphere) and hydrothermal vents and also input from space. While the former is perhaps better known and more commonly taught in school, we now know that comet and asteroid dust deliver tons of organics to the Earth every day, therefore this flux of reduced carbon from space probably also played a role in making the Earth habitable. We will compare and contrast the types and abundances of organics from on and off the Earth given standard assumptions. Perhaps each process provided specific compounds (amino acids, sugars, amphiphiles) that were directly related to the origin or early evolution of life. In any case, whether planetary, nebular or interstellar, we will consider how one might attempt to distinguish between abiotic organic molecules from actual signs of life as part of a robotic search for life in the Solar System.     

The origin of the biologically coded amino acids

Biology uses essentially 20 amino acids for its coded protein enzymes, representing a very small subset of the structurally possible set. Most models of the origin of life suggest organisms developed from environmentally available organic compounds. A variety of amino acids are easily produced under conditions which were believed to have existed on the primitive Earth or in the early solar nebula. The types of amino acids produced depend on the conditions which prevailed at the time of synthesis, which remain controversial. The selection of the biological set is likely due to chemical and early biological evolution acting on the environmentally available compounds based on their chemical properties. Once life arose, selection would have proceeded based on the functional utility of amino acids coupled with their accessibility by primitive metabolism and their compatibility with other biochemical processes. Some possible mechanisms by which the modern set of 20 amino acids was selected starting from prebiotic chemistry are discussed.     

Carbonaceous Micrometeorites and the Origin of Life

Giant micrometeorites (sizes ranging from >50 to 500 m), such as those that were first recovered from clean pre-industrial Antarctic ices in December 1987, represent by far the dominant source of extraterrestrial carbonaceous material accreted by the Earth's surface, about 50 000 times the amount delivered by meteorites (sizes a few cm). They correspond to large interplanetary dust particles that survived unexpectedly well their hypervelocity impact with the Earth's atmosphere, contrary to predictions of theoretical models of such impacts. They are related to relatively rare groups of carbonaceous chondrites (2% of the meteorite falls) and not to the most abundant meteorites (ordinary chondrites and differentiated micrometeorites). About 80% of them appear to be highly unequilibrated fine-grained assemblages of mineral grains, where an abundant carbonaceous component is closely associated on a scale of 0.1 m to both hydrous and anhydrous minerals, including potential catalysts. These observations suggest that micrometeorites could have functioned as individual microscopic chemical reactors to contribute to the synthesis of prebiotic molecules on the early Earth, about 4 billions years ago. The recent identification of some of their complex organics (amino acids and polycyclic aromatic hydrocarbons), and the observation that they behave as very efficient cosmochromatographs, further support this early carbonaceous micrometeorite scenario. Future prospects include identifying the host phases (probably ferrihydrite) of their complex organics, evaluating their catalytic activity, and assessing whether synergetic interactions between micrometeorites and favorable zones of the early Earth (such as submarine hydrothermal vents) accelerated and/or modified such synthesis.     

Molten Earth and the origin of prebiological molecules

Evidence for the molten Earth at its accretion time has been accumulated through the geochemical investigations and the observations of the surfaces of planets by space probes such as Venera 8, Mariner 9, Surveyor, Luna, and Apollo. The primitive terrestrial atmosphere might have been derived from the volcanic gases, as suggested by Rubey, but of a higher temperature than so far assumed. A thermochemical calculation of the composition of the volcanic gas suggests the following possibilities:

1. Large amounts of H₂ and CO were present in the primitive atmosphere. This gives a theoretical basis for the HCN-production experiment by Abelson.
2. HCHO and NH₃ existed in the primitive oceans, of the amount comparable with the weight of the present biosphere.
3. Plenty of NO ₃ ⁻ , SO ₄ ⁻⁻ , and PO ₄ ⁻⁻⁻ were expected in the primitive oceans. The NO ₃ ⁻ ions might have been useful for the nitrate respiration advocated by Egami.

In an appendix, it is argued, on the basis of the observational evidence of the exospheric temperatures of planets by space probes, that a highly reducing atmosphere would (if it existed on the primitive Earth) have disappeared very quickly due to the thermal escape of hydrogen from its exosphere.     

Dynamic Co-evolution of Peptides and Chemical Energetics, a Gateway to the Emergence of Homochirality and the Catalytic Activity of Peptides

We propose a scenario for the dynamic co-evolution of peptides and energy on the primitive Earth. From a multi component system consisting of hydrogen cyanide, several carbonyl compounds, ammonia, alkyl amine, carbonic anhydride, borate and isocyanic acid, we show that the reversibility of this system leads to several intermediate nitriles, that irreversibly evolve to alpha-amino acids and N-carbamoyl amino acids via selective catalytic processes. On the primitive Earth these N-carbamoyl amino acids combined with energetic molecules (NOx) may have been the core of a molecular engine producing peptides permanently and assuring their recycling and evolution. We present this molecular engine, a production example, and its various selectivities. The perspectives for such a dynamic approach to the emergence of peptides are evoked in the conclusion.     

Conformational relationships between amino acids and their anticodons in the primitive decoding system

Detailed calculations of the conformational characteristics of a primitive decoding system are presented. A penta-nucleotide serves as the primitive tRNA (PIT) with a triplet of primitive anticodon (PAC) in a helical conformation. This molecular moiety has a cleft in the middle. An amino acid can comfortably nestle into the cleft. The conformation of this molecular association is stabilised by a few hydrogen bonds. The stereochemistry of the moiety restricts the conformational possibilities and the sidechain of the amino acid gets oriented at a proper position and in the correct direction to interact intimately with the PAC in the middle of the PIT. The model favours L-amino acids for beta-D-ribonucleotides. The location of the sidechain of the amino acid in the PIT gives a raison d'être for the important features of the organisation of nucleotide triplets for amino acids in the Genetic Code. The interaction of a few key amino acids with the different combinations of bases as PAC sequences has been studied and the stereochemical basis for the selection of the anticodons for amino acids is elucidated.     

Molten earth and the origin of prebiological molecules.

Evidence for the molten Earth at its accretion time has been accumulated through the geochemical investigations and the observations of the surfaces of planets by space probes such as Venera 8, Mariner 9, Surveyor, Luna, and Apollo. The primitive terrestrial atmosphere might have been derived from the volcanic gases, as suggested by Rubey, but of a higher temperature than so far assumed. A thermochemical calculation of the composition of the volcanic gas suggests the following possibilities: (1) Large amounts of H2 and CO were present in the primitive atmosphere. This gives a theoretical basis for the HCN-production experiment by Abelson. (2) HCHO and NH3 existed in the primitive oceans, of the amount comparable with the weight of the present biosphere. (3) Plenty of NO3-, SO4, and PO4 were expected in the primitive oceans. The NO3- ions might have been useful for the nitrate respiration advocated by Egami. In an appendix, it is argued, on ;he basis of the observational evidence of the exospheric temperatures of planets by space probes, that a highly reducing atmosphere would (if it existed on the primitive Earth) have disappeared very quickly due to the thermal escape of hydrogen from its exosphere.     

Transformation of some hydroxy amino acids to other amino acids.

It has been observed that beta-hydroxy-alpha-amino acids are transformed into other amino acids, when heated in dilute solutions with phosphorous acid, phosphoric acid or their ammonium salts. It has been shown that as in the case of previously reported glycine-aldehyde reactions, glycine also reacts with acetone to give beta-hydroxyvaline under prebiologically feasible conditions. It is suggested, therefore, that the formation of beta-hydroxy-alpha-amino acids and their transformation to other amino acids may have been a pathway for the synthesis of amino acids under primitive earth conditions.     

Inhibition of Rare Earth Catalytic Activity by Proteins

Catalytic action of rare earth element, Ce(IV) to hydrolyzephosphomonoester bonds was confirmed. This effect wasconsidered to suppress abiotic synthesis ofnucleotides and nucleic acids in the primitive sea,and hence the origin of life. However, we found thatthe presence of proteins, especially albumin, stronglyinhibited the catalytic action of Ce(IV). Thisfinding was supported by preferential binding of rare earthelements (REEs) to proteins which was revealed using the radioisotopes of these REEs. Consequently, if a large amount ofproteins was synthesized in the primitive sea, abioticsynthesis of phosphomonoester compounds, and hencenucleic acids, might have been possible.     

Comet impacts and chemical evolution on the bombarded Earth

Amino acids yields for previously published shock tube experiments are used with minimum Cretaceous-Tertiary (K/T) impactor mass and comet composition to predict AIB amino acid K/T boundary sediment column density. The inferred initial concentration of all amino acids in the K/T sea and in similar primordial seas just after 10 km comet impacts would have been at least 10^–7 M. However, sinks for amino acids must also be considered in calculating amino acid concentrations after comet impacts and in assessing the contribution of comets to the origin of life. The changing concentration of cometary amino acids due to ultraviolet light is compared with the equilibrium concentration of amino acids produced in the sea from corona discharge in the atmosphere, deposition in water, and degradation by ultraviolet light. Comets could have been more important than endogenous agents for initial evolution of amino acids. Sites favorable for chemical evolution of amino acids are examined and it is concluded that chemical evolution could have occurred at or above the surface even during periods of intense bombardment of Earth before 3.8 billion years ago.     

The Organic Composition of Carbonaceous Meteorites: The Evolutionary Story Ahead of Biochemistry

Carbon-containing meteorites provide a natural sample of the extraterrestrial organic chemistry that occurred in the solar system ahead of life''s origin on the Earth. Analyses of 40 years have shown the organic content of these meteorites to be materials as diverse as kerogen-like macromolecules and simpler soluble compounds such as amino acids and polyols. Many meteoritic molecules have identical counterpart in the biosphere and, in a primitive group of meteorites, represent the majority of their carbon. Most of the compounds in meteorites have isotopic compositions that date their formation to presolar environments and reveal a long and active cosmochemical evolution of the biogenic elements. Whether this evolution resumed on the Earth to foster biogenesis after exogenous delivery of meteoritic and cometary materials is not known, yet, the selective abundance of biomolecule precursors evident in some cosmic environments and the unique L-asymmetry of some meteoritic amino acids are suggestive of their possible contribution to terrestrial molecular evolution.     

Biomarkers as Tracers for Life on Early Earth and Mars

Biomarkers in geological samples are products derived from biochemical (natural product) precursors by reductive and oxidative processes (e.g., cholestanes from cholesterol). Generally, lipids, pigments and biomembranes are preserved best over longer geological times and labile compounds such as amino acids, sugars, etc. are useful biomarkers for recent times. Thus, the detailed characterization of biomarker compositions permits the assessment of the major contributing species of extinct and/or extant life. In the case of the early Earth, work has progressed to elucidate molecular structure and carbon isotopic signals preserved in ancient sedimentary rocks. In addition, the combination of bacterial biochemistry with the organic geochemistry of contemporary and ancient hydrothermal ecosystems permits the modeling of the nature, behavior and preservation potential of primitive microbial communities. This approach uses combined molecular and isotopic analyses to characterize lipids produced by cultured bacteria (representative of ancient strains) and to test a variety of culture conditions which affect their biosynthesis. On considering Mars, the biomarkers from lipids and biopolymers would be expected to be preserved best if life flourished there during its early history (3.5–4 × 10⁹ yr ago). Both oxidized and reduced products would be expected. This is based on the inferred occurrence of hydrothermal activity during that time with the concomitant preservation of biochemically-derived organic matter. Both known biomarkers (i.e., as elucidated for early terrestrial samples and for primitive terrestrial microbiota) and novel, potentially unknown compounds should be characterized.     

Formation of amino acids on heating glycine with alumina

The conversion of glycine into amino acids on heating at 240°C with basic manganous carbonate and alumina is investigated. Alanine, -aminobutyric acid, norvaline, norleucine, sarcosine, N-ethylglycine, N-methylalanine, N-ethylalanine, aspartic acid and glutamic acid are identified among the products of the reaction. Paper chromatography, ion-exchange chromatography and nuclear magnetic resonance are used for the analysis. A scheme for the observed transformations is presented and it is suggested that it may have been a pathway for the synthesis of amino acids from glycine under primitive Earth conditions.