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Ribose and related sugars from ultraviolet irradiation of interstellar ice analogs

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Science  08 Apr 2016:
Vol. 352, Issue 6282, pp. 208-212
DOI: 10.1126/science.aad8137

Making ribose in interstellar ices

Astrobiologists have long speculated on the origin of prebiotic molecules such as amino acids and sugars. Meinert et al. demonstrated that numerous prebiotic molecules can be formed in an interstellar-analog sample containing a mixture of simple ices of water, methanol, and ammonia. They irradiated the sample with ultraviolet light under conditions similar to those expected during the formation of the solar system. This yielded a wide variety of sugars, including ribose—a major constituent of ribonucleic acid (RNA).

Science, this issue p. 208

Abstract

Ribose is the central molecular subunit in RNA, but the prebiotic origin of ribose remains unknown. We observed the formation of substantial quantities of ribose and a diversity of structurally related sugar molecules such as arabinose, xylose, and lyxose in the room-temperature organic residues of photo-processed interstellar ice analogs initially composed of H2O, CH3OH, and NH3. Our results suggest that the generation of numerous sugar molecules, including the aldopentose ribose, may be possible from photochemical and thermal treatment of cosmic ices in the late stages of the solar nebula. Our detection of ribose provides plausible insights into the chemical processes that could lead to formation of biologically relevant molecules in suitable planetary environments.

DNA is the genetic source code for all known living organisms. It is currently thought that DNA evolved from a primordial ribonucleic acid RNA world state (1, 2), in which ribose chemically binds and orientates the complementary purine and pyrimidine nucleobases for efficient base pairing. Ribose thereby forms the essential part of the RNA backbone. However, ribose is difficult to form, and the source of the ribose subunits in the sugars that constitute the key stereodictating elements in nucleic acid structure remained unknown (3, 4). We describe here the identification of precursor molecules, including ribose, in simulated precometary ices using the sensitive two-dimensional gas chromatography time-of-flight mass spectrometry (GC×GC-TOFMS) technique.

Our astrophysical scenario involves the simulation of the photo- and thermo-chemistry of precometary ices. It is based on the assumption that planetesimals (including asteroids, comets, and the parent bodies of meteorites) were formed in the solar nebula from the aggregation of icy grains already present and processed at the late molecular cloud stages. This also took place within the protoplanetary disk phase, owing to vertical/radial mixing of the protostellar materials (5). As a model, these dust particles are composed of silicate (or carbon) grains surrounded by icy mantles containing H2O, CH3OH, NH3, and other volatile species (6). In this environment, dust particles and icy mantles are expected to be subjected to ultraviolet photons and cosmic-ray irradiation, leading to a complex chemistry in the condensed phase. We empirically simulated this process in the laboratory at low temperature (T = 78 K) and low pressure (p = 10−7 mbar). Volatile molecules H2O, 13CH3OH, and NH3 in a 10:3.5:1 ratio were condensed on the cooled surface, while being irradiated with ultraviolet photons, and then warmed up to room temperature, leading to the formation of an organic residue (7). 13C isotopic labeling of the methanol allowed us to distinguish between the reaction products and potential contamination during manipulation of the sample and through the analytical procedure. A precise description of the experimental setup is provided in the supplementary materials.

The samples were extracted with water, derivatized, and submitted to GC×GC-TOFMS analysis (8). The analytical multidimensional separation apparatus consisted of a 0.25-mm capillary column with a β-cyclodextrin stationary phase in the first dimension and a polyethylene glycol capillary column of 100 μm inner diameter in the second dimension. A cryogenic modulator connected both capillary columns (7). A reflectron time-of-flight (TOF) mass spectrometer has been used for recording retention times and mass spectra. The GC×GC-TOFMS analysis in combination with our derivatization protocol (7) provided the simultaneous resolution and identification of the sugar and sugar-related compounds, which has not been possible with classical chromatographic devices because of coelution of analytes.

We detected aldoses and ketoses in these simulated interstellar ice analogs as schematically represented by the Fischer projections in Fig. 1. The monosaccharides ribose, arabinose, xylose, and lyxose belong to the aldopentoses; ribulose and xylulose are ketopentoses. The aldopentoses were resolved and identified in both α- and β-pyranose form (Fig. 2), and the ketopentoses show ketol form. Besides aldopentoses and ketopentoses, we identified the ketotetrose erythrulose. Mass spectra of the analytes and the interpretation of characteristic fragmentation pathways leading to unambiguous identification are provided (supplementary text), along with details on the quantification of the analytes.

Fig. 1 Aldoses and ketoses as identified in a sample generated under simulated precometary conditions.

The structures of sugar alcohols, monosaccharides, and saccharinic acids are indicated along with the amount of the identified analyte in the simulated ice sample. Identified C-6 analytes are not included. The Fischer projections indicate the d-enantiomer form only. ppm, parts per million by mass;q.l., quantification limit;d.l., detection limit.

Fig. 2 Multidimensional gas chromatogram showing ribose and other monosaccharides in the organic residue from an evolved precometary ice analog.

See also fig. S1 and movie S1 (7). The atomic mass units 206 and 294 were selected for the multidimensional chromatographic representation. d- and l-enantiomers of the monosaccharides were not resolved.

The corresponding saccharinic acids (sugar acids) were identified. We also detected the corresponding sugar alcohols, along with threitol, erythritol, mannitol, and sorbitol. We further found the related series of hydroxycarboxylic acids.

A systematic representation of the identified molecular species is given in Table 1, which indicates the analytes’ retention times in the first and second chromatographic dimension and mass spectra of analyzed sample and standard. The analytes detected in the organic residue were found to contain 13C isotopes, whereas the standard samples used for identification were made of the natural isotopic composition dominated by 12C (figs. S3 to S5). We therefore exclude experimental contamination and conclude that all described analytes were formed by the H2O, 13CH3OH, and NH3 volatile reactants that were deposited under simulated interstellar precometary conditions (fig. S2).

Table 1 Identified sugars and related organic compounds in interstellar ice analogs initially composed of H2O:13CH3OH:NH3.

#C, quantity of carbon atoms; Rt1, GC×GC retention time 1st dimension; Rt2, GC×GC retention time 2nd dimension.

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The molecular complexity in the evolved ices reported here suggests a far larger similarity to meteoritic organic materials than previously assumed. Thus, molecular evolution of meteoritic organic species available for planetary environments could have benefited from accretion of protostellar material. The sugars, dicarboxylic acids, C-4 hydroxycarboxylic acids, and branched-chain molecules described here have not previously been identified, although aldehydes, including glycolaldehyde and glyceraldehyde, have been found in similar laboratory residues (9), along with lower hydroxycarboxylic acids (10). Sugar-related alcohols and acids have previously been detected in the Murchison meteorite (11). Glycolaldehyde has been found sublimating from the nucleus of comet Lovejoy (C/2014 Q2) (12) and by means of millimeter-wave rotational transitions in emission toward the Galactic center source Sagittarius B2(N) (13). Glycolaldehyde was recently also detected in solar-type protostars (14). Moreover, glycolaldehyde and ethylene glycol were characterized by means of infrared spectroscopy in radiation chemistry of laboratory ices (15).

The diversity of sugar molecules formed from H2O, 13CH3OH, and NH3 under interstellar conditions can be understood in the framework of a photochemically initiated formose-type reaction. Reactant and intermediate species of the formose reaction (1618) are formaldehyde and glycolaldehyde that undergo aldol condensations to produce hydroxyl aldehydes and hydroxyl ketones with linear and branched structures (Fig. 3 and fig. S6). As in our case, sugar alcohols and sugar acids typically accompany the sugars formed by the formose reaction. We further detected the branched chain molecules hydroxymethylglycerol and hydroxymethyltetritol, which indicate a formose-type reaction mechanism (19, 20). The classical formose reaction is known to require a divalent metal catalyst such as Ca2+, Pb2+, or Tl2+ for the stabilizing effect of chelating ions on enediols (18), a condition not needed in the present work. Final steps of the formose-type reaction might have occurred above 78 K during temperature increase of the sample to room temperature, in which reactants diffuse and react within the labile and sublimating ice matrix.

Fig. 3 The formose reaction.

Formaldehyde 1 condenses under autocatalytic reaction kinetics to form glycolaldehyde 2, which undergoes an aldol reaction by forming glyceraldehyde 3. Dihydroxyacetone 4 is formed by aldose-ketose isomerization of 3 and reacts with 2, forming pentulose 5, which isomerizes to an aldopentose 6 such as ribose. In an alternative pathway, dihydroxyacetone 4 reacts with 1, producing ketotetrose 7 and aldotetrose 8 (18).

The parts-per-million values of the photoproducts described in Fig. 1 sum up to greater than 35,000 (table S1), which corresponds to a value >3.5% (by mass) (7). Thus, sugars, sugar alcohols, and sugar acids are present notably above trace or ultratrace quantities and are therefore considered major molecular constituents of the condensed interstellar organics. The relative yield of ribose, which is known to be very small in the classical formose reaction, resulted in higher values during our cold scenario. We regard this result as central for an implication for prebiotic chemistry because it shows that even at this initial level of molecular “simplicity,” we observe an autocatalytic reaction. This, in turn, may be interpreted as a link between astrochemistry and astrobiology. The acquisition of kinetic data and enantioseparation will be necessary to rationalize the reaction mechanism of the sugar formation and to search for asymmetric autocatalytic effects.

The identification of ribose in the organic residues obtained from evolved precometary ices does not necessarily indicate the prebiotic evolutionary pathway. Besides ribose, we identified threose in its oxidized and reduced form, threonic acid and threitol, respectively. Threose is the molecular component of threose nucleic acid (TNA), a nucleic acid analog discussed to have preceded RNA (21). We further detected glycol and glycerol, which provide the molecular backbones of glycol and glycerol nucleic acids (GNAs) (22, 23). The molecular building blocks of peptide nucleic acids (PNAs), N-(2-aminoethyl)glycine and 2,4-diaminobutanoic acid, were previously detected in organic residues from similar ice experiments (24). In this experimental frame, precursors of both proteins (amino acids) (25) and genetic material (sugars and their derivatives) are produced in large amounts so that if delivered from meteorites in the Earth’s environment, their coevolution may be considered one of the standing issues in prebiotic chemistry (26).

Our samples are fully soluble in water (as well as in other polar solvents), a condition that is essential for any further prebiotic activity. In aqueous solution, sugar molecules, including ribose, develop chemical equilibria between the open form (Fig. 1), the cyclic furanose and pyranose forms (Fig. 2), and in between the various constitutional isomers such as ribose and arabinose. Our experiments demonstrate plausible physical and chemical environmental conditions that allow for abiotic ribose synthesis.

Our findings support the identification of organic molecules in cometary samples taken in situ by the Philae Lander (27, 28) part of the cometary Rosetta mission (29). Our analytical results demonstrate the usefulness of multidimensional chromatographic techniques for the chemical analyses of extraterrestrial samples, which are often available only in small quantities, in which sugar molecules including ribose may be present.

Supplementary Materials

www.sciencemag.org/content/352/6282/208/suppl/DC1

Materials and Methods

Supplementary Text

Figs. S1 to S6

Table S1

Movie S1

References (3045)

References and Notes

  1. Materials and methods are available as supplementary materials on Science Online.
  2. Acknowledgments: This work was funded by the Agence Nationale de la Recherche grant ANR-12-IS07-0006 and Consejo Nacional de Ciencia y Tecnología (CONACYT) grant C001-CONACYT-ANR-188689. L.L.S.d’H. thanks the Centre National d’Études Spatiales for the continuous support of the MICMOC (Matière Interstellaire et Cométaire: Molécules Organiques Compexes) experiment. The data obtained in this study are available through the open archive HAL (hal-01278288, https://hal.archives-ouvertes.fr).
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