The missing organic molecules on Mars

Abstract

The missing organic molecules on Mars

Steven A. Benner*, Kevin G. Devine, Lidia N. Matveeva, and David H. Powell

Departments of Chemistry, Anatomy, and Cell Biology, University of Florida, Gainesville, FL 32611

Communicated by Leslie Orgel, The Salk Institute for Biological Studies, San Diego, CA, December 13, 1999 (received for review November 4, 1998)

GC-MS on the Viking 1976 Mars missions did not detect organic molecules on the Martian surface, even those expected from meteorite bombardment. This result suggested that the Martian regolith might hold a potent oxidant that converts all organic molecules to carbon dioxide rapidly relative to the rate at which they arrive. This conclusion is influencing the design of Mars missions. We reexamine this conclusion in light of what is known about the oxidation of organic compounds generally and the nature of organics likely to come to Mars via meteorite. We conclude that nonvolatile salts of benzenecarboxylic acids, and perhaps oxalic and acetic acid, should be metastable intermediates of meteoritic organics under oxidizing conditions. Salts of these organic acids would have been largely invisible to GC-MS. Experiments show that one of these, benzenehexacarboxylic acid (mellitic acid), is generated by oxidation of organic matter known to come to Mars, is rather stable to further oxidation, and would not have been easily detected by the Viking experiments. Approximately 2 kg of meteorite-derived mellitic acid may have been generated per m2 of Martian surface over 3 billion years. How much remains depends on decomposition rates under Martian conditions. As available data do not require that the surface of Mars be very strongly oxidizing, some organic molecules might be found near the surface of Mars, perhaps in amounts sufficient to be a resource. Missions should seek these and recognize that these complicate the search for organics from entirely hypothetical Martian life.

(Keywords:) Viking | organic compounds | exobiology | astrobiology

 

Source: Proc. Natl. Acad. Sci. USA Vol. 97, Issue 6, 2425-2430, March 14, 2000


Article

The Viking 1976 missions to Mars performed several experiments designed to assess the potential for life on the planet. The results were puzzling. Samples of soil from the top 10 cm of the Martian surface released dioxygen when exposed to humidity (1). At least one compound in a set of radiolabeled organic compounds (formate, D,L-lactate, glycolate, glycine, and D,L-alanine) released radiolabeled carbon dioxide when placed in aqueous solution on the Martian surface, evidently via oxidative processes (2). Both results were initially thought to indicate the presence of life. However, a GC-MS experiment looking for volatile products from a sample of soil heated for 30 s (sometimes repeatedly) at 200°, 350°, and 500°C did not detect any organic molecules (3). This result was (and remains) strong evidence against life on Mars, at least at the surface.

The failure to detect organic molecules by GC-MS was especially surprising, because some 2.4 × 108 g of reduced carbon comes to Mars each year via meteor (Table 1; refs. 4-6). Many meteoritic organic compounds are volatile and should have been detected by GC-MS (7). Pyrolysis should have generated volatile products from many of the nonvolatile compounds, including the polymeric organic substance known as "kerogen," which accounts for the majority of organic material coming to Mars via meteorite and as much as 1-3% of the weight of some meteorites (8). These products too should have been detected by Viking but were not.

These results have been interpreted as evidence that the Martian surface contains no organic molecules of any kind, presumably because the Martian regolith carries an oxidant powerful enough to convert all organics to carbon dioxide. Coupled with the absence of liquid water on the surface of Mars and with the irradiation of the surface by ultraviolet light, the failure to detect organic substances led many to conclude that one must dig deeply (and perhaps very deeply) below the Martian surface to have a chance of encountering any organic molecules that may have arisen from life on Mars (perhaps present several billion years ago, when the surface of Mars was more like the surface of Earth at that time and when life almost certainly had emerged on Earth) or of encountering organic molecules that may have been delivered to Mars via meteorite (9, 10).

Because this interpretation is influencing the design of missions to Mars, it is timely to reexamine it in light of what is known about the oxidation of organic compounds generally, the nature of organic substances likely to come to Mars, and the features of the Viking 1976 analysis that determined the kinds of organic molecules that it could have detected. The examination suggests that organic compounds that arrive on Mars via meteorite are most likely to be converted to carboxylic acid derivatives that would not be easily detected by GC-MS. Organic molecules generated on Mars itself by nonbiological (11-14) or (entirely hypothetical) biological synthesis (15) should suffer similar fates at or near the surface.

The Generic Oxidation Pathway. As in any organic reaction, the specific oxidant, specific ambient conditions, and specific catalysts determine what intermediates will accumulate in the oxidative degradation of organic compounds on Mars. Only by missions to Mars can we learn these specifics to decide what has actually happened to meteoritic organics and, by inference, to other organics that might have come to the Martian surface.

Because we must today design missions to do that, we must extract as much as possible from general knowledge of organic reactivity and experimental data obtained in terrestrial laboratories under "non-Martian" conditions (very often in liquid water) to make a best guess as to how organic molecules will be transformed on the Martian surface. To this end, we infer here some generic pathways for the oxidation of organic molecules on Mars. As substrates for these pathways, we consider meteoritic organics, because this assumption avoids the need to presume the presence of organic compounds from Martian life.

We begin with the fact that the surface of Mars is exposed to ultraviolet radiation with sufficient energy to cleave water to give H· and HO· radicals. Some of the H· radicals must recombine to give dihydrogen (H2), which escapes into space (16, 17). This process leaves behind the HO· radical, which could react directly with organic substances, dimerize to give H2O2 (18), or generate peroxides or other oxidizing species through combination with elements in the Martian soil.

The HO· radical reacts directly with most organic molecules. In aqueous solution under terrestrial conditions, the second order rate constants range from 107 to 1010 liter·mol-1·s-1 for reactions that include hydrogen atom abstractions and additions to double bonds (19). The concentration of HO· on Mars is 1 × 105 to 2 × 105 cm-3, a number similar to the concentration of HO· radical in the atmosphere at the surface of Earth (17).

Let us consider five types of organic compounds (Table 1) known to come to Mars via meteorites: alkanes, alkylbenzenes, naphthalene and higher polycyclic aromatic hydrocarbons, kerogen, and amino acids and hydroxyacids. We shall ask how HO· and H2O2 might transform these in generic oxidation pathways and whether metastable intermediates in these pathways might accumulate.

Alkanes. Alkanes react generically with the HO· radical via abstraction of a hydrogen radical (H·) at a tertiary center (preferentially), then a secondary center, and last a primary center. This relative reactivity reflects the relative stability of the radical products and occurs under a wide range of conditions. Thus, a straight chain alkane would lose an internal hydrogen in the generic mechanism (Fig. 1A).

The resulting secondary radical is extremely reactive and will be trapped by almost anything available. It will react with another HO· radical to yield a secondary alcohol. It can transfer an electron to (for example) Fe3+, generating a carbocation that can be trapped by water (for example, from a hydrated mineral), also generating the secondary alcohol. Other products are possible, but a secondary alcohol is the generic intermediate in the oxidative degradation of n-alkanes (Fig. 1A).

HO· abstracts an H· from the carbon attached to the alcohol oxygen more readily than it abstracts H· from the parent alkene. Thus, the secondary alcohol (under generic conditions) is expected to react faster than the parent. It will therefore not accumulate but yield a ketone. The ketone, in turn, should undergo further oxidation to generate an ester, which will be cleaved to give a carboxylic acid and a primary alcohol, which will be oxidized directly to another carboxylic acid. Alternatively, the ketone might enolize, suffer oxidation, and then lead to a fragmentation to generate two carboxylic acids (Fig. 1A).

By these steps, the generic oxidation pathway for alkanes leads to carboxylic acids. These are, of course, subject to further oxidation. The abstraction of an H· from the carbon attached to the COOH group is expected to be an important mode of oxidation involving HO·. This oxidation will ultimately generate the next shorter carboxylic acid. Depending on the trap, the product would be an alkane (and the process would resume) or another more easily oxidized derivative.

In this cascade of intermediates, the carboxylic acid is the first that is slower to degrade than to be formed. Under typical Fenton conditions, for example, acetic acid reacts with the HO· radical 100 times more slowly than does ethanol (19). Carboxylic acids are therefore likely to accumulate. Further, acetate is more stable to further reaction under generic conditions than propanoic acid and longer alkylcarboxylic acids. Thus, acetic acid accumulates especially effectively.

Exemplifying the generic oxidation pathway are some "brand name" oxidations. In a Kuhn-Roth oxidation, for example, an alkane is refluxed in a solution of concentrated chromic acid (20). Insignificant amounts of ketone or alcohol products can be isolated as intermediates in the oxidation cascade that follows; these are too unstable with respect to further oxidation. Organic alkanecarboxylic acids (butanoic acid and propanoic acid, for example) can be isolated as metastable intermediates, however. On incubation for longer times, these are further degraded to acetic acid. Acetic acid too can be oxidized to give carbon dioxide. Nevertheless, acetate is more stable than longer chain alkanecarboxylic acids and accumulates. This accumulation makes the Kuhn-Roth oxidation useful for elucidating the structure of natural products. The amount of acetate produced from a known amount of alkane corresponds to the number of methyl groups in the alkane.

Alkylbenzenes. The HO· radical abstracts a benzylic H· from the alkyl group of alkylbenzenes (such as toluene) to give a rather stable benzyl radical (Fig. 1B). This radical may trap HO· or lose an electron to Fe3+ and then trap water, in each case forming benzyl alcohol. Benzyl alcohol is more reactive than toluene under generic conditions. It is not expected to accumulate but rather to be converted to benzaldehyde. Benzaldehyde is also unstable with respect to further oxidation and also should not accumulate in the generic process. Rather, it should be converted to benzoic acid.

Benzoic acid no longer has a benzylic hydrogen to lose to a radical oxidant. It is still thermodynamically unstable in the presence of oxidants to conversion to carbon dioxide. But it is metastable, resists further oxidation, and accumulates. Because benzoic acid has no hydrogen on the carbon adjacent to the COOH group, it also lacks a path available to alkanecarboxylic acids for further oxidative degradation. Further generic oxidative degradation involves a one-electron oxidation of the benzoate anion, which decarboxylates to yield the phenyl radical, which then can be converted to benzene or phenol.

This generic pathway can be illustrated by a specific oxidative process with commercial importance. Benzoic acid is synthesized on ton scales via the oxidation of toluene. The stability of benzoic acid under these oxidizing conditions is sufficient to allow benzoic acid to accumulate in the industrial process (21).

Naphthalene and higher polycyclic aromatic hydrocarbons. The generic oxidation of polycyclic aromatic hydrocarbons involves the addition of the HO· radical to give a hydroxycyclohexadienyl radical. This radical suffers further oxidation to give eventually single core aromatic rings to which carboxylic acids are attached wherever a second ring was fused. Thus, naphthalene, phenanthrene (22), and anthracene (23) all give phthalic acid in the generic oxidation process. Higher polycyclic aromatic hydrocarbons give benzenetricarboxylic, tetracarboxylic, pentacarboxylic, and hexacarboxylic acids (Fig. 1; ref. 24).

The generic pathway can be exemplified with laboratory reactions of naphthalene, which is 1-6 ppm in some carbonaceous chondrites (25). The pseudo first-order rate constant for the first step in the reaction between naphthalene and the HO· radical (Fig. 2) is 0.035 min-1 (26). The rate constants for further oxidation of 1- and 2-naphthol are higher (0.88 and 0.27 min-1). These higher rate constants imply that neither 1- nor 2-naphthol will accumulate. The metastable end products are phthaldehyde and phthalic acid.

Analogous outcomes are observed under a variety of other conditions [oxidation catalyzed by TiO2, by SiO2 (27), and by Fe2O3 (28)]. This uniformity in outcome argues that the oxidation of naphthalene will generically yield phthalic acid as a metastable intermediate (29). The metastability of phthalic acid to further oxidation has commercial significance. An important industrial synthesis of phthalic acid begins with the oxidation of naphthalene (30). Phthalic acid is also produced from naphthalene under simulated Martian conditions (31).

Kerogen. Polymeric organic material (kerogen) has no defined structure. On Earth, kerogen (coal, for example) comes via metamorphosis of biological matter. Under generic oxidation conditions, the aromatic portions of kerogen generate benzenecarboxylic acids, with one carboxylic acid group for every position on the core benzene ring that was attached to a carbon in the parent structure. These are metastable, accumulate, and are isolated and quantitated when defining the structure of kerogens. For example, treating coal with alkaline permanganate oxidized its carbon to carbonic acid (H2CO3, 42% vol/vol), acetic acid (CH3COOH, 2% vol/vol), oxalic acid (HOOC-COOH, 7% vol/vol), and benzenecarboxylic acids (48% vol/vol), with a trace of succinic acid (HOOC-CH2-CH2-COOH; ref. 32). Kerogen is the most abundant organic substance in meteorites. As with terrestrial kerogen, the kerogen from the Murchison meteorite gives benzenecarboxylic acid products when oxidized (33, 34). These are stable in refluxing nitric acid for 27 h.

 Amino acids and hydroxyacids. Polyfunctional molecules are easier to oxidize than unfunctionalized carboxylic acids. Thus, hydrogen peroxide (a mild oxidant) will, in the presence of iron salts, catalyze the oxidative decarboxylation of alpha-hydroxyacids to give carbon dioxide and the shorter aldehyde. This reaction, well known in sugar chemistry, has a brand name (the "Ruff degradation;" ref. 35).

Polyfunctionalized compounds are more rapidly converted to carbon dioxide under generic oxidation conditions. Oxalic acid is likely to be metastable, however, where iron is abundant (36).

The Amounts and Fates of Organic Carboxylic Acids. This discussion makes the case that aromatic and aliphatic carboxylic acids are the metastable products of generic oxidation of meteoritic organic compounds. The generic oxidation pathway is exemplified by so many specific (admittedly terrestrial) reactions and is so well supported by organic structure theory that it seems plausible that it is followed on Mars as well.

If meteorites bring 2.4 × 108 g/year of organic carbon to Mars (4) and the mass yield of benzenecarboxylic acid from this material is 10%, then approx7.2 × 1016 g of benzenecarboxylic acids should have been generated on Mars since its surface dried 3 billion years ago. The surface area of Mars is 3.6 × 1013 m2, corresponding to 2 kg of benzenecarboxylic acids per m2 of the Martian surface.

What would be the fate of these organic molecules? It is certain that these compounds were diluted by wind and impact into the Martian regolith. The meteoritic kerogen would have been accompanied by at least 70 times more inorganic meteoritic material. The inorganic composition of meteorites is very different than from that of a range of carbonaceous chondrites. These data provide a minimum measure of dilution. If mixed in the regolith to a depth of 1 m, 2 kg of benzenecarboxylates would contribute approx500 ppm by weight of the first meter of surface of Mars (the density of Mars is approx4 g/cm3). If gardening mixes the material to a depth of 1 km, benzenecarboxylates will be present at a concentration of 500 ppb. Analytical tools sensitive to the ppb level should detect these.

Other processes might have removed organic carboxylic acids from the immediate surface. Carboxylic acids react with metal oxides to form salts (37, 38). These often have some solubility in water. If the Martian surface has been exposed to water in the past, organic salts may have been removed from the surface by leaching and concentrated in subsurface environments. Examples on Earth include highly soluble salts (e.g., halite) and poorly soluble salts (e.g., gypsum). This process is almost certainly less important than gardening in the recent past, because surface water on Mars has been scarce for billions of years, and iron salts of benzenecarboxylic acids are poorly soluble (39, 40).

Most important, of course, are chemical reactions that would degrade the carbon skeleton. The Fenton reaction serves as a model, even recognizing that