Results and Discussion

We investigated the abundance and distribution of nucleobases and nucleobase analogs in 11 different carbonaceous chondrites from three different groups (CI, CM, and CR) representing the entire range of aqueous alteration (types 1, 2, and 3) and one ureilite meteorite. Eleven out of the 12 meteorites studied contained at least the nucleobase adenine. The three CM2 carbonaceous chondrites (Murchison, LEW 90500, and LON 94102) particularly stood out because they had the most diverse and abundant set of purines measured (Fig. 1 and SI Text). Total purine abundances were 4 to 12 times higher in CM2 carbonaceous chondrites compared to the other meteorites examined. As the degree of aqueous alteration increases in CM carbonaceous chondrites, the overall abundance and diversity of nucleobases decreases as seen in ALH 83100 (CM1/2), SCO 06043 (CM1), and MET 01070 (CM1). Meteorites of other groups (CI and CR) with varying degrees of aqueous alteration (types 1, 2, and 3) also had comparatively less total purine abundance and structurally diversity compared to CM2 carbonaceous chondrites. Furthermore, there is an apparent correlation between purine diversity and the diversity of other small organic species, such as amino acids (5), with the maximum diversity found in CM2 carbonaceous chondrites. Interestingly, this correlation does not hold for the abundances of such compounds; for example, CR2 and CR3 meteorites are rich in amino acids and small amines (5, 20, 21) but poor in purines. Based on our measurements, the CM2 carbonaceous chondrites appear to have provided a more favorable environment for the formation and/or preservation of purines compared to other types of carbonaceous chondrites.

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Fig. 1.

Distribution of guanine, hypoxanthine, xanthine, adenine, purine, and 2,6-diaminopurine in 11 carbonaceous chondrites and one ureilite. The three CM2 carbonaceous chondrites in this study (Murchison, LEW 90500, and LON 94102) contained significantly higher (approximately 4× to 12×) abundances of purine nucleobases as well as greater structurally diversity. The * represents a tentative assignment. The meteorites are roughly ordered by increasing aqueous alteration (Right to Left) as determined using mineralogical and isotopic evidence (38–41). The relative degree of aqueous alteration among carbonaceous chondrites within the same group and of the same petrologic type is less certain, although some ordering can be made.

Establishing an unambiguous extraterrestrial origin for any biological nucleobase in carbonaceous chondrites is challenging. Unlike meteoritic amino acids, nucleobases are achiral so enantiomeric ratios (i.e., D/L ratios) cannot be used to help distinguish between abiotic and biotic origins. With sample-limited meteorites, compound-specific stable isotope analysis may be impractical or impossible due to the large amount of meteorite material required. Additionally, other meteoritic organics may prevent an unambiguous stable isotope ratio measurement despite extensive sample cleanup and chromatography (19). Indigenous organic compounds in meteorites are usually present in structurally homologous series (2); therefore, finding nucleobase analogs not typically found in terrestrial biochemistry would strongly support an extraterrestrial origin for these canonical nucleobases because they are often produced concurrently in abiotic syntheses.

Purine, 2,6-diaminopurine, and 6,8-diaminopurine were unambiguously identified in LON 94102 (Fig. 2) and a larger extract of Murchison by their chromatographic retention time, accurate mass spectrum (including accurate mass measurements on multiple fragmentation products), and coinjection with standards (resulting in the detection of a single peak) (22). Additionally, two different formic acid extracts of LON 94102 were analyzed on three different liquid chromatography–mass spectrometry instruments (one triple quadrupole and two Orbitraps) in two separate laboratories [National Aeronautics and Space Administration (NASA) Goddard Space Flight Center and Thermo Scientific], which all produced similar results. Purine and 6,8-diaminopurine were identified (by their chromatographic retention time and an accurate mass measurement for the parent mass) in several other meteorites as well (Fig. 1 and SI Text). This demonstrates that both purine and 6,8-diaminopurine are widely distributed in carbonaceous chondrites, particularly in CM2 and CR2 meteorites, and provides additional support that purines found in these meteorites are indigenous and not terrestrial contaminants. Aside from one report of 2,6-diaminopurine occurring in cyanophage S-2L (23), these three purines are rare or absent in terrestrial biology. Studies of 8-aminoadenosine, as a potential cancer therapeutic, have shown that this compound is known to inhibit transcription by multiple mechanisms (24) so that the presence of 6,8-diaminopurine (8-aminoadenine) in meteorites is highly unlikely to be the result of terrestrial biological contamination.

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Fig. 2.

Mass-selected fragmentation spectra of reference standards (left spectra) and compounds found in the meteorite LON 94102 (right spectra) measured on an LTQ Orbitrap XL hybrid mass spectrometer using an HCD (higher energy collision dissociation) setting of 90 to 100%. Purine, adenine, 2,6-diaminopurine, and 6,8-diaminopurine were identified using accurate mass measurements on the parent mass and multiple fragment masses and chromatographic retention time. Mass accuracy of less than 5 ppm allows for the unambiguous assignment of elemental formulae. The * represents inferences in the fragmentation spectra that are present in both the meteorite and reference standard spectra.

All of the purines observed in Murchison and LON 94102 (i.e., adenine, guanine, hypoxanthine, xanthine, purine, 2,6-diaminopurine, and 6,8-diaminopurine) were also generated from aqueous reactions of NH₄CN (see SI Text). Adenine (normalized to 1) was the most abundant nucleobase in the formic acid extracted NH₄CN samples followed by purine (0.79), hypoxanthine (0.23), 6,8-diaminopurine (0.07, assuming the same response factor as 2,6-diaminopurine), 2,6-diaminopurine (0.05), guanine (0.02), and xanthine (0.01). Although the relative abundances of these purines are different than those detected in carbonaceous chondrites, this may be attributable to the extensive aqueous and energetic processing the asteroid parent bodies have undergone during their approximately 4.5 billion-year history (25) compared to the NH₄CN reactions. The presence of hydrogen cyanide and ammonia as synthetic precursor molecules has been deduced in hydrated carbonaceous chondrites based on the presence of α-amino acids, α-hydroxy acids, and iminodicarboxylic acids reported in the Murchison meteorite, which supports a Strecker-type synthesis requiring hydrogen cyanide and ammonia (13, 26–29). Additionally, abundant ammonia has been detected in the CR2 carbonaceous chondrite GRA 95229 after hydrothermal treatment (30), which was one of the meteorites in our study.

Purine, 2,6-diaminopurine, and 6,8-diaminopurine were not detected (above our parts-per-billion detection limits) in the procedural blanks, nucleobase procedural samples, serpentine control samples, Murchison soil sample (see SI Text), or Antarctic ice sample (see SI Text), which strongly suggests that these compounds are indigenous to the meteorites. Because adenine, guanine, hypoxanthine, and xanthine were observed in both the soil and Antarctic ice samples (though at different ratios and lower abundances than observed in meteorites; see SI Text), it could still be argued that these nucleobases are the result of terrestrial contamination. On the other hand, these same nucleobases are also synthesized concurrently with purine, 2,6-diaminopurine, and 6,8-diaminopurine in reactions of NH₄CN. Furthermore, the distributions of purines measured in the nine Antarctic meteorites appear to correlate with meteorite petrology and the extent of parent body alteration rather than with the content of the terrestrial environments from which they were recovered, arguing against terrestrial contamination from the ice. Based on the elevated abundances of these compounds in the meteorites compared with terrestrial sources, we propose that the adenine, guanine, hypoxanthine, and xanthine observed in CM2 meteorites are largely extraterrestrial, but could potentially also contain traces of terrestrial contamination.

The presence of extraterrestrial purines in meteorites has far-reaching implications. The first cellular systems on the early Earth were presumably assembled from three components: nucleic acids, proteins, and cell membranes (31). Potential molecular subunits for constructing all of these macromolecular species (e.g., amino acids, amphiphilic compounds, and from this study—a variety of purine nucleobases) have been identified in meteorites and appear to be indigenous. Thus, meteorites may have served as a molecular kit providing essential ingredients for the origin of life on Earth and possibly elsewhere.

The identification of purine, 2,6-diaminopurine, and 6,8-diaminopurine in the meteorites Murchison and LON 94102 also expands the inventory of nucleobases that could have been available during the origins of life. The stability of 2,6-diaminopurine is similar to that of adenine, guanine, and xanthine and the accumulation of these compounds on the early Earth may have been possible (32). Furthermore, 2,6-diaminopurine can base pair with uracil (or thymine), and the additional amino group permits the formation of three hydrogen bonds (33). Because meteorites may have provided a significant source of prebiotic organic material including purines, it is plausible that alternative nucleobases such as 2,6-diaminopurine, 6,8-diaminopurine, xanthine, and hypoxanthine were available for constructing the first genetic molecules. It has been proposed that an “expanded genetic alphabet” was present, and perhaps required, in the RNA World (34); conversely an all-purine primitive RNA has also been proposed (35).