Abiotic formation of alkylsulfonic acids in interstellar analog ices and implications for their detection on Ryugu.

For the last century, the source of sulfur in Earth's very first organisms has remained a fundamental, unsolved enigma. While sulfates and their organic derivatives with sulfur in the S(+VI) oxidation state represent core nutrients in contemporary biochemistry, the limited bioavailability of sulfates during Earth's early Archean period proposed that more soluble S(+IV) compounds served as the initial source of sulfur for the first terrestrial microorganisms. Here, we reveal via laboratory simulation experiments that the three simplest alkylsulfonic acids-water soluble organic S(+IV) compounds-can be efficiently produced in interstellar, sulfur-doped ices through interaction with galactic cosmic rays. This discovery opens a previously elusive path into the synthesis of vital astrobiological significance and untangles fundamental mechanisms of a facile preparation of sulfur-containing, biorelevant organics in extraterrestrial ices; these molecules can be eventually incorporated into comets and asteroids before their delivery and detection on Earth such as in the Murchison, Tagish Lake, and Allende meteorites along with the carbonaceous asteroid Ryugu.

Resolution and quantification of carbohydrates by enantioselective comprehensive two-dimensional gas chromatography.

Carbohydrates, in particular the d-enantiomers of ribose, 2-deoxyribose, and glucose, are essential to life's informational biopolymers (RNA/DNA) and for supplying energy to living cells through glycolysis. Considered to be potential biosignatures in the search of past or present life, our capacity to detect and quantify these essential sugars is crucial for future space missions to the Moon, Mars or Titan as well as for sample-return missions. However, the enantioselective analysis of carbohydrates is challenging and both research and routine applications, are lacking efficient methods that combine highly sensitive and reproducible detection with baseline enantioselective resolution and reliable enantiomeric excess (ee) measurements. Here, we present four different derivatization strategies in combination with multidimensional gas chromatography coupled to a reflectron time-of-flight mass spectrometer (GC×GC-TOF-MS) for the enantioselective resolution of C3 to C6 carbohydrates potentially suitable for sample-return analyses. Full mass spectral interpretation and calibration curves for one single-step (cyclic boronate derivatives) and three two-step derivatization protocols (aldononitrile-acetate, hemiacetalization-trifluoroacetylation, and hemiacetalization-permethylation) are presented for concentrations ranging from 1 to 50 pmol µL⁻1 with correlation coefficients R2 > 0.94. We compared several analytical parameters including reproducibility, sensitivity (LOD and LOQ), overall separation, chiral resolution (RS), mass spectrum selectivity, stability during long term storage, and reliability of ee measurements to guide the application-dependent selection of optimal separation and quantification performance.

Chiroptical properties of membrane glycerophospholipids and their chiral backbones.

Glycerophospholipid membranes are one of the key cellular components. Still, their species-dependent composition and homochirality remain an elusive subject. In the context of the astrophysical circularly polarized light scenario likely involved in the generation of a chiral bias in meteoritic amino and sugar acids in space, and consequently in the origin of life's homochirality on Earth, this study reports the first measurements of circular dichroism and anisotropy spectra of a selection of glycerophospholipids, their chiral backbones and their analogs. The rather low asymmetry in the interaction of UV/VUV circularly polarized light with sn-glycerol-1/3-phosphate indicates that chiral photons would have been unlikely to directly induce symmetry breaking to membrane lipids. In contrast, the anisotropy spectra of d-3-phosphoglyceric acid and d-glyceraldehyde-3-phosphate unveil up to 20 and 100 times higher maximum anisotropy factor values, respectively. This first experimental report, targeted on investigating the origins of phospholipid symmetry breaking, opens up new avenues of research to explore alternative mechanisms leading to membrane lipid homochirality, while providing important clues for the search for chiral biosignatures of extant and/or extinct life in space, in particular for the ExoMars 2028 mission.

Uncovering the chiral bias of meteoritic isovaline through asymmetric photochemistry.

Systematic enrichments of L-amino acids in meteorites is a strong indication that biological homochirality originated beyond Earth. Although still unresolved, stellar UV circularly polarized light (CPL) is the leading hypothesis to have caused the symmetry breaking in space. This involves the differential absorption of left- and right-CPL, a phenomenon called circular dichroism, which enables chiral discrimination. Here we unveil coherent chiroptical spectra of thin films of isovaline enantiomers, the first step towards asymmetric photolysis experiments using a tunable laser set-up. As analogues to amino acids adsorbed on interstellar dust grains, CPL-helicity dependent enantiomeric excesses of up to 2% were generated in isotropic racemic films of isovaline. The low efficiency of chirality transfer from broadband CPL to isovaline could explain why its enantiomeric excess is not detected in the most pristine chondrites. Notwithstanding, small, yet consistent L-biases induced by stellar CPL would have been crucial for its amplification during aqueous alteration of meteorite parent bodies.

Fast and precise chiroptical spectroscopy by photoelectron elliptical dichroism.

The photoionization of chiral molecules by elliptically polarized femtosecond laser pulses produces photoelectron angular distributions which show a strong and enantio-sensitive forward/backward asymmetry along the light propagation direction. We report on high precision measurements of this photoelectron elliptical dichroism (PEELD). Using an optical cavity to recycle the laser pulses and increase the signal-to-noise ratio, we determine enantiomeric excesses with a 0.04% precision with a low-power femtosecond laser (4 W) in a compact scheme. We perform momentum-resolved PEELD measurements in 16 molecules, from volatile terpenes to non-volatile amino acids and large iodoarenes. The results demonstrate the high structural sensitivity of PEELD, confirming the spectroscopic interest of this technique. Last, we show how a convolutional neural network can be used to retrieve the chemical and enantiomeric composition of a sample from the momentum-resolved PEELD maps.

Processing of methane and acetylene ices by galactic cosmic rays and implications to the color diversity of Kuiper Belt objects.

Kuiper Belt objects exhibit a wider color range than any other solar system population. The origin of this color diversity is unknown, but likely the result of the prolonged irradiation of organic materials by galactic cosmic rays (GCRs). Here, we combine ultrahigh-vacuum irradiation experiments with comprehensive spectroscopic analyses to examine the color evolution during GCR processing methane and acetylene under Kuiper Belt conditions. This study replicates the colors of a population of Kuiper Belt objects such as Makemake, Orcus, and Salacia. Aromatic structural units carrying up to three rings as in phenanthrene (C14H10), phenalene (C9H10), and acenaphthylene (C12H8), of which some carry structural motives of DNA and RNA connected via unsaturated linkers, were found to play a key role in producing the reddish colors. These studies demonstrate the level of molecular complexity synthesized of GCR processing hydrocarbon and hint at the role played by irradiated ice in the early production of biological precursor molecules.

Biological effects of the loss of homochirality in a multicellular organism.

Homochirality is a fundamental feature of all known forms of life, maintaining biomolecules (amino-acids, proteins, sugars, nucleic acids) in one specific chiral form. While this condition is central to biology, the mechanisms by which the adverse accumulation of non-L-α-amino-acids in proteins lead to pathophysiological consequences remain poorly understood. To address how heterochirality build-up impacts organism's health, we use chiral-selective in vivo assays to detect protein-bound non-L-α-amino acids (focusing on aspartate) and assess their functional significance in Drosophila. We find that altering the in vivo chiral balance creates a 'heterochirality syndrome' with impaired caspase activity, increased tumour formation, and premature death. Our work shows that preservation of homochirality is a key component of protein function that is essential to maintain homeostasis across the cell, tissue and organ level.

Chiroptical activity of gas-phase propylene oxide predicting the handedness of interstellar circular polarization in the presolar nebula.

Propylene oxide, the first chiral molecule recently detected in the interstellar medium, has once again raised the question whether biomolecular chirality might have cosmic origins. However, accurate chiroptical properties of propylene oxide in the ultraviolet spectral range necessary to suggest possible asymmetric synthetic routes in the gas phase are scarce. Here, we report on the first experimental measurements of the anisotropy spectra of gas-phase propylene oxide in the vacuum ultraviolet spectral range. Our experimental results provide novel insights into the handedness of interstellar circular polarization at the dawn of molecular evolution of our star- and planet-forming region. Besides the fundamental importance of this new investigation for understanding the origin and evolution of homochirality on Earth, our high-resolution experimental electronic circular dichroism data will inspire new efforts in quantum computational spectroscopy.

Resolution, quantification, and reliable determination of enantiomeric excess of proteinogenic and non-proteinogenic amino acids by comprehensive two-dimensional gas chromatography.

This work proposes a comprehensive two-dimensional gas chromatography method for the resolution and quantification of 27 amino acids, including 17 enantiomeric pairs, as stable N-trifluoroacetyl-O-methyl ester derivatives. The derivatization approach in combination with enantioselective two-dimensional gas chromatography has proven to be highly responsive with a method detection limit of 1-7 pg even for sterically hindered amino acids such as α,α-dialkylated, and N-alkylated amino acids. Accurate determination of the enantiomeric excess was achieved with errors in the range of ±0.5%-2.5% (1σ) at concentrations ≥10-6 M. A thorough study of the mass spectra of the amino acid derivatives allowed the fragmentation pathways to be distinguished, enabling chromatographic peaks to be unambiguously assigned. The proposed method is particularly suited for applications that require the precise determination of enantiomeric excesses such as those concerning the role of d-amino acid enantiomers in humans, animals, and the environment, as well as for analyses of extraterrestrial samples aimed at understanding the selection of amino acids in stereochemical l-configuration.

Amino acid gas phase circular dichroism and implications for the origin of biomolecular asymmetry.

Life on Earth employs chiral amino acids in stereochemical L-form, but the cause of molecular symmetry breaking remains unknown. Chiroptical properties of amino acids - expressed in circular dichroism (CD) - have been previously investigated in solid and solution phase. However, both environments distort the intrinsic charge distribution associated with CD transitions. Here we report on CD and anisotropy spectra of amino acids recorded in the gas phase, where any asymmetry is solely determined by the genuine electromagnetic transition moments. Using a pressure- and temperature-controlled gas cell coupled to a synchrotron radiation CD spectropolarimeter, we found CD active transitions and anisotropies in the 130-280 nm range, which are rationalized by ab initio calculation. As gas phase glycine was found in a cometary coma, our data may provide insights into gas phase asymmetric photochemical reactions in the life cycle of interstellar gas and dust, at the origin of the enantiomeric selection of life's L-amino acids.

Concentration and pH effect on the electronic circular dichroism and anisotropy spectra of aqueous solutions of glyceric acid calcium salt.

Electronic circular dichroism (ECD) and anisotropy spectra carry information on differential absorption of left- and right-circularly polarized light (LCPL and RCPL) by optically active compounds. This makes them powerful tools for the rapid determination of enantiomeric excesses (ee) in asymmetric synthetic and pharmaceutical chemistry, as well as for predicting the ee inducible by ultraviolet (UV) CPL. The ECD response of a chiral molecule is, however, critically dependent on the properties of the surrounding medium. Here, we report on the first ECD/anisotropy spectra of aqueous solutions of the calcium salt dihydrate of glyceric acid. A systematic study of the effect of the salt concentration and pH on the chiroptical response revealed significant changes and the appearance of a new ECD band of opposite sign. Based on the literature, this can be rationalized by the increase in the relative proportion of free glyceric acid/glycerate to Ca2+ complexes with glycerate with decreasing salt concentration or pH. Glyceric acid can be readily produced under astrophysical conditions. The anisotropy spectra of the solution containing prevalently the free form of this dihydroxy carboxylic acid resemble the ones of previously investigated aliphatic chain hydroxycarboxylic acids and proteinogenic amino acids. This indicates possible common handedness of stellar CPL-induced asymmetry in the potential comonomers of primitive proto-peptides.

Racemate Resolution of Alanine and Leucine on Homochiral Quartz, and Its Alteration by Strong Radiation Damage.

Homochiral proteins orchestrate biological functions throughout all domains of life, but the origin of the uniform l-stereochemistry of amino acids remains unknown. Here, we describe enantioselective adsorption experiments of racemic alanine and leucine onto homochiral d- and l-quartz as a possible mechanism for the abiotic emergence of biological homochirality. Substantial racemate resolution with enantiomeric excesses of up to 55% are demonstrated to potentially occur in interstitial pores, along grain boundaries or small fractures in local quartz-bearing environments. Our previous hypothesis on the enhanced enantioselectivity due to uranium-induced fission tracks could not be validated. Such capillary tubes in the near-surface structure of quartz have been proposed to increase the overall chromatographic separation of enantiomers, but no systematic positive correlation of accumulated radiation damage and enantioselective adsorption was observed in this study. In general, the natural l-quartz showed stronger enantioselective adsorption affinities than synthetic d-quartz without any significant trend in amino acid selectivity. Moreover, the l-enantiomer of both investigated amino acids alanine and leucine was preferably adsorbed regardless of the handedness of the enantiomorphic quartz sand. This lack of mirror symmetry breaking is probably due to the different crystal habitus of the synthetic z-bar of d-quartz and the natural mountain crystals of l-quartz used in our experiments.

Chiroptical activity of hydroxycarboxylic acids with implications for the origin of biological homochirality.

Circularly polarised light (CPL) interacting with interstellar organic molecules might have imparted chiral bias and hence preluded prebiotic evolution of biomolecular homochirality. The L-enrichment of extra-terrestrial amino acids in meteorites, as opposed to no detectable excess in monocarboxylic acids and amines, has previously been attributed to their intrinsic interaction with stellar CPL revealed by substantial differences in their chiroptical signals. Recent analyses of meteoritic hydroxycarboxylic acids (HCAs) - potential co-building blocks of ancestral proto-peptides - indicated a chiral bias toward the L-enantiomer of lactic acid. Here we report on novel anisotropy spectra of several HCAs using a synchrotron radiation electronic circular dichroism spectrophotometer to support the re-evaluation of chiral biomarkers of extra-terrestrial origin in the context of absolute photochirogenesis. We found that irradiation by CPL which would yield L-excess in amino acids would also yield L-excess in aliphatic chain HCAs, including lactic acid and mandelic acid, in the examined conditions. Only tartaric acid would show "unnatural" D-enrichment, which makes it a suitable target compound for further assessing the relevance of the CPL scenario.

Biosignature Analysis of Mars Soil Analogs from the Atacama Desert: Challenges and Implications for Future Missions to Mars.

The detection of biosignatures on Mars is of outstanding interest in the current field of astrobiology and drives various fields of research, ranging from new sample collection strategies to the development of more sensitive detection techniques. Detailed analysis of the organic content in Mars analog materials collected from extreme environments on Earth improves the current understanding of biosignature preservation and detection under conditions similar to those of Mars. In this article, we examined the biological fingerprint of several locations in the Atacama Desert (Chile), which include different wet and dry, and intermediate to high elevation salt flats (also named salars). Liquid chromatography and multidimensional gas chromatography mass spectrometry measurement techniques were used for the detection and analysis of amino acids extracted from the salt crusts and sediments by using sophisticated extraction procedures. Illumina 16S amplicon sequencing was used for the identification of microbial communities associated with the different sample locations. Although amino acid load and organic carbon and nitrogen quantities were generally low, it was found that most of the samples harbored complex and versatile microbial communities, which were dominated by (extremely) halophilic microorganisms (most notably by species of the Archaeal family Halobacteriaceae). The dominance of salts (i.e., halites and sulfates) in the investigated samples leaves its mark on the composition of the microbial communities but does not appear to hinder the potential of life to flourish since it can clearly adapt to the higher concentrations. Although the Atacama Desert is one of the driest and harshest environments on Earth, it is shown that there are still sub-locations where life is able to maintain a foothold, and, as such, salt flats could be considered as interesting targets for future life exploration missions on Mars.

Origin of alkylphosphonic acids in the interstellar medium.

For decades, the source of phosphorus incorporated into Earth's first organisms has remained a fundamental, unsolved puzzle. Although contemporary biomolecules incorporate P(+V) in their phosphate moieties, the limited bioavailability of phosphates led to the proposal that more soluble P(+III) compounds served as the initial source of phosphorus. Here, we report via laboratory simulation experiments that the three simplest alkylphosphonic acids, soluble organic phosphorus P(+III) compounds, can be efficiently generated in interstellar, phosphine-doped ices through interaction with galactic cosmic rays. This discovery opens a previously overlooked avenue into the formation of key molecules of astrobiological significance and untangles basic mechanisms of a facile synthesis of phosphorus-containing organics in extraterrestrial ices, which can be incorporated into comets and asteroids before their delivery and detection on Earth such as in the Murchison meteorite.

The Astrophysical Formation of Asymmetric Molecules and the Emergence of a Chiral Bias.

The biomolecular homochirality in living organisms has been investigated for decades, but its origin remains poorly understood. It has been shown that circular polarized light (CPL) and other energy sources are capable of inducing small enantiomeric excesses (ees) in some primary biomolecules, such as amino acids or sugars. Since the first findings of amino acids in carbonaceous meteorites, a scenario in which essential chiral biomolecules originate in space and are delivered by celestial bodies has arisen. Numerous studies have thus focused on their detection, identification, and enantiomeric excess calculations in extraterrestrial matrices. In this review we summarize the discoveries in amino acids, sugars, and organophosphorus compounds in meteorites, comets, and laboratory-simulated interstellar ices. Based on available analytical data, we also discuss their interactions with CPL in the ultraviolet (UV) and vacuum ultraviolet (VUV) regions, their abiotic chiral or achiral synthesis, and their enantiomeric distribution. Without doubt, further laboratory investigations and upcoming space missions are required to shed more light on our potential extraterrestrial molecular origins.

An interstellar synthesis of phosphorus oxoacids.

Phosphorus signifies an essential element in molecular biology, yet given the limited solubility of phosphates on early Earth, alternative sources like meteoritic phosphides have been proposed to incorporate phosphorus into biomolecules under prebiotic terrestrial conditions. Here, we report on a previously overlooked source of prebiotic phosphorus from interstellar phosphine (PH3) that produces key phosphorus oxoacids-phosphoric acid (H3PO4), phosphonic acid (H3PO3), and pyrophosphoric acid (H4P2O7)-in interstellar analog ices exposed to ionizing radiation at temperatures as low as 5 K. Since the processed material of molecular clouds eventually enters circumstellar disks and is partially incorporated into planetesimals like proto Earth, an understanding of the facile synthesis of oxoacids is essential to untangle the origin of water-soluble prebiotic phosphorus compounds and how they might have been incorporated into organisms not only on Earth, but potentially in our universe as well.

d-Amino acids in molecular evolution in space - Absolute asymmetric photolysis and synthesis of amino acids by circularly polarized light.

Living organisms on the Earth almost exclusively use l-amino acids for the molecular architecture of proteins. The biological occurrence of d-amino acids is rare, although their functions in various organisms are being gradually understood. A possible explanation for the origin of biomolecular homochirality is the delivery of enantioenriched molecules via extraterrestrial bodies, such as asteroids and comets on early Earth. For the asymmetric formation of amino acids and their precursor molecules in interstellar environments, the interaction with circularly polarized photons is considered to have played a potential role in causing chiral asymmetry. In this review, we summarize recent progress in the investigation of chirality transfer from chiral photons to amino acids involving the two major processes of asymmetric photolysis and asymmetric synthesis. We will discuss analytical data on cometary and meteoritic amino acids and their potential impact delivery to the early Earth. The ongoing and future ambitious space missions, Hayabusa2, OSIRIS-REx, ExoMars 2020, and MMX, are scheduled to provide new insights into the chirality of extraterrestrial organic molecules and their potential relation to the terrestrial homochirality. This article is part of a Special Issue entitled: d-Amino acids: biology in the mirror, edited by Dr. Loredano Pollegioni, Dr. Jean-Pierre Mothet and Dr. Molla Gianluca.

Enantioresolution and quantification of monosaccharides by comprehensive two-dimensional gas chromatography.

This work presents the development of a simple and efficient analytical protocol for the direct enantioselective resolution of sugars. A racemic mixture of the C3 sugar d,l-glyceraldehyde and the C5 monosaccharides d,l-arabinose, d,l-ribose, d,l-xylose, and d,l-lyxose was subjected to derivatization with trifluoroacetic anhydride, and corresponding derivatives were separated on a ß-cyclodextrin column with excellent resolution factors. Even though each aldopentose shows beside the linear form four predominant cyclic hemiacetals being the α- and ß-furanose along with the α- and ß-pyranose, we show that the overall enantiomeric excess of each compound can be precisely determined. Moreover, the measured detection limit for derivatized aldopentoses ranges from 0.015 to 0.019pmol on the column, while the quantification limit varies from 0.5 to 0.64pmol on the column.

Response to Comment on "Ribose and related sugars from ultraviolet irradiation of interstellar ice analogs".

We detected ribose and related sugars in the organic residues of simulated interstellar ices using multidimensional gas chromatography. Kawai questions the formation of sugar compounds in the ices and suggests that they arise from a classical formose reaction during sample workup for analysis. We disagree with this hypothesis and present additional data to argue that Kawai's criticism does not apply.