Prebiotic Context Research Articles

Cosmic dust fertilization of glacial prebiotic chemistry on early Earth

AbstractEarth’s surface is deficient in available forms of many elements considered limiting for prebiotic chemistry. In contrast, many extraterrestrial rocky objects are rich in these same elements. Limiting prebiotic ingredients may, therefore, have been delivered by exogenous material; however, the mechanisms by which exogeneous material may be reliably and non-destructively supplied to a planetary surface remains unclear. Today, the flux of extraterrestrial matter to Earth is dominated by fine-grained cosmic dust. Although this material is rarely discussed in a prebiotic context due to its delivery over a large surface area, concentrated cosmic dust deposits are known to form on Earth today due to the action of sedimentary processes. Here we combine empirical constraints on dust sedimentation with dynamical simulations of dust formation and planetary accretion to show that localized sedimentary deposits of cosmic dust could have accumulated in arid environments on early Earth, in particular glacial settings that today produce cryoconite sediments. Our results challenge the widely held assumption that cosmic dust is incapable of fertilizing prebiotic chemistry. Cosmic dust deposits may have plausibly formed on early Earth and acted to fertilize prebiotic chemistry.

Crystallization as a selection force at the polymerization of nucleotides in a prebiotic context

Accumulation and selection of nucleotides is one of the most challenging problems surrounding the origin of the first RNA molecules on our planet. In the current work we propose that guanosine 3',5' cyclic monophosphate could selectively crystallize upon evaporation of an acidic prebiotic pool containing various other nucleotides. The conditions of the evaporative crystallization are fully compatible with the subsequent acid catalyzed polymerization of this cyclic nucleotide reported in earlier studies and may be relevant in a broad range of possible prebiotic environments. Albeit cytidine 3',5' cyclic monophosphate has the ability to selectively accumulate under the same conditions, its crystal structure is not likely to support polymer formation.

Elemental sulfur, hydrogen sulfide, and carbon monoxide-driven dimerization of glycine at sub-millimolar concentrations: Implications for the origin of life

The life’s origin in submarine hydrothermal systems is a long-standing scenario supported by diverse scientific disciplines, while verification of its chemical plausibility remains a major bottleneck. Most scenarios of hydrothermal origin postulate peptides as key players in prebiotic chemistry; nevertheless, it remains unknown how peptides were formed from geochemically available amino acids that must be low in concentration. Here we show that a simple mixing with elemental sulfur (S0), hydrogen sulfide (HS–), and carbon monoxide (CO) enables an effective dimerization of glycine (Gly) at micro to several millimolar concentrations. Incubation of 1 mM Gly with the three inorganic compounds in a warm alkaline solution (pH 9.3 and 35 or 50 °C) led up to 18% conversion of Gly to glycylglycine (GlyGly). Dimerization of 0.01 mM Gly was also discerned in the yield far exceeding the thermodynamic equilibrium (0.4% yield). In this reaction, CO is oxidized to CO2 concomitant with the reduction of S0 to polysulfides, serving as the driving force for the Gly-to-GlyGly conversion. Although the formation of CO2 as a byproduct suppressed the formation of GlyGly, its adverse effect was mitigated by carbonate precipitation upon adding Mg2+ and Ca2+. To our knowledge, 0.01 mM is the lowest concentration of amino acid oligomerized experimentally in the prebiotic context. Given the ubiquity of S0, HS–, and CO in primordial ocean hydrothermal systems, and the abundance of Mg2+ and Ca2+ in seawater, our demonstrated favorable condition for amino acid dimerization is likely to have occurred on the Hadean seafloor. This possibility supports an abiotic appearance of peptides and thereby facilitates the hydrothermal origin of life.

The Origin of Translation: Bridging the Nucleotides and Peptides.

Extant biology uses RNA to record genetic information and proteins to execute biochemical functions. Nucleotides are translated into amino acids via transfer RNA in the central dogma. tRNA is essential in translation as it connects the codon and the cognate amino acid. To reveal how the translation emerged in the prebiotic context, we start with the structure and dissection of tRNA, followed by the theory and hypothesis of tRNA and amino acid recognition. Last, we review how amino acids assemble on the tRNA and further form peptides. Understanding the origin of life will also promote our knowledge of artificial living systems.

Net Charges of the Ribosomal Proteins of the S10 and spc Clusters of Halophiles Are Inversely Related to the Degree of Halotolerance.

ABSTRACTNet positive charge(s) on ribosomal proteins (r-proteins) have been reported to influence the assembly and folding of ribosomes. A high percentage of r-proteins from extremely halophilic archaea are known to be acidic or even negatively charged. Those proteins that remain positively charged are typically far less positively charged. Here, the analysis is extended to non-archaeal halophilic bacteria, eukaryotes, and halotolerant archaea. The net charges (pH 7.4) of the r-proteins that comprise the S10-spc operon/cluster from individual microbial and eukaryotic genomes were estimated and intercompared. It was observed that, as a general rule, the net charges of individual proteins remained mostly basic as the salt tolerance of the bacterial strains increased from 5 to 15%. The most striking exceptions were the extremely halophilic bacterial strains, Salinibacter ruber SD01, Acetohalobium arabaticum DSM 5501 and Selenihalanaerobacter shriftii ATCC BAA-73, which are reported to require a minimum of 18% to 21% salt for their growth. All three strains have higher numbers of acidic S10-spc cluster r-proteins than what is seen in the moderate halophiles or the halotolerant strains. Of the individual proteins, only uL2 never became acidic. uS14 and uL16 also seldom became acidic. The net negative charges on several of the S10-spc cluster r-proteins are a feature generally shared by all extremely halophilic archaea and bacteria. The S10-spc cluster r-proteins of halophilic fungi and algae (eukaryotes) were exceptions: these were positively charged despite the halophilicity of the organisms.IMPORTANCE The net charges (at pH 7.4) of the ribosomal proteins (r-proteins) that comprise the S10-spc cluster show an inverse relationship with the halophilicity/halotolerance levels in both bacteria and archaea. In non-halophilic bacteria, the S10-spc cluster r-proteins are generally basic (positively charged), while the rest of the proteomes in these strains are generally acidic. On the other hand, the whole proteomes of the extremely halophilic strains are overall negatively charged, including the S10-spc cluster r-proteins. Given that the distribution of charged residues in the ribosome exit tunnel influences cotranslational folding, the contrasting charges observed in the S10-spc cluster r-proteins have potential implications for the rate of passage of these proteins through the ribosomal exit tunnel. Furthermore, the universal protein uL2, which lies in the oldest part of the ribosome, is always positively charged irrespective of the strain/organism it belongs to. This has implications for its role in the prebiotic context.

Polyamines Mediate Folding of Primordial Hyperacidic Helical Proteins.

Polyamines are known to mediate diverse biological processes, and specifically to bind and stabilize compact conformations of nucleic acids, acting as chemical chaperones that promote folding by offsetting the repulsive negative charges of the phosphodiester backbone. However, whether and how polyamines modulate the structure and function of proteins remain unclear. In particular, early proteins are thought to have been highly acidic, like nucleic acids, due to a scarcity of basic amino acids in the prebiotic context. Perhaps polyamines, the abiotic synthesis of which is simple, could have served as chemical chaperones for such primordial proteins? We replaced all lysines of an ancestral 60-residue helix-bundle protein with glutamate, resulting in a disordered protein with 21 glutamates in total. Polyamines efficiently induce folding of this hyperacidic protein at submillimolar concentrations, and their potency scaled with the number of amine groups. Compared to cations, polyamines were several orders of magnitude more potent than Na+, while Mg2+ and Ca2+ had an effect similar to that of a diamine, inducing folding at approximately seawater concentrations. We propose that (i) polyamines and dications may have had a role in promoting folding of early proteins devoid of basic residues and (ii) coil–helix transitions could be the basis of polyamine regulation in contemporary proteins.

Prebiotic Peptide Bond Formation Through Amino Acid Phosphorylation. Insights from Quantum Chemical Simulations.

Condensation reactions between biomolecular building blocks are the main synthetic channels to build biopolymers. However, under highly diluted prebiotic conditions, condensations are thermodynamically hampered since they release water. Moreover, these reactions are also kinetically hindered as, in the absence of any catalyst, they present high activation energies. In living organisms, in the formation of peptides by condensation of amino acids, this issue is overcome by the participation of adenosine triphosphate (ATP), in which, previous to the condensation, phosphorylation of one of the reactants is carried out to convert it as an activated intermediate. In this work, we present for the first time results based on density functional theory (DFT) calculations on the peptide bond formation between two glycine (Gly) molecules adopting this phosphorylation-based mechanism considering a prebiotic context. Here, ATP has been modeled by a triphosphate (TP) component, and different scenarios have been considered: (i) gas-phase conditions, (ii) in the presence of a Mg2+ ion available within the layer of clays, and (iii) in the presence of a Mg2+ ion in watery environments. For all of them, the free energy profiles have been fully characterized. Energetics derived from the quantum chemical calculations indicate that none of the processes seem to be feasible in the prebiotic context. In scenarios (i) and (ii), the reactions are inhibited due to unfavorable thermodynamics associated with the formation of high energy intermediates, while in scenario (iii), the reaction is inhibited due to the high free energy barrier associated with the condensation reactions. As a final consideration, the role of clays in this TP-mediated peptide bond formation route is advocated, since the interaction of the phosphorylated intermediate with the internal clay surfaces could well favor the reaction free energies.

When the Surface Matters: Prebiotic Peptide‐Bond Formation on the TiO2 (101) Anatase Surface through Periodic DFT‐D2 Simulations

The mechanism of the peptide-bond formation between two glycine (Gly) molecules has been investigated by means of PBE-D2* and PBE0-D2* periodic simulations on the TiO2 (101) anatase surface. This is a process of great relevance both in fundamental prebiotic chemistry, as the reaction univocally belongs to one of the different organizational events that ultimately led to the emergence of life on Earth, as well as from an industrial perspective, since formation of amides is a key reaction for pharmaceutical companies. The efficiency of the surface catalytic sites is demonstrated by comparing the reactions in the gas phase and on the surface. At variance with the uncatalyzed gas-phase reaction, which involves a concerted nucleophilic attack and dehydration step, on the surface these two steps occur along a stepwise mechanism. The presence of surface Lewis and Brönsted sites exerts some catalytic effect by lowering the free energy barrier for the peptide-bond formation by about 6 kcal mol-1 compared to the gas-phase reaction. Moreover, the co-presence of molecules acting as proton-transfer assistants (i.e., H2 O and Gly) provide a more significant kinetic energy barrier decrease. The reaction on the surface is also favorable from a thermodynamic standpoint, involving very large and negative reaction energies. This is due to the fact that the anatase surface also acts as a dehydration agent during the condensation reaction, since the outermost coordinatively unsaturated Ti atoms strongly anchor the released water molecules. Our theoretical results provide a comprehensive atomistic interpretation of the experimental results of Martra et al. (Angew. Chem. Int. Ed. 2014, 53, 4671), in which polyglycine formation was obtained by successive feedings of Gly vapor on TiO2 surfaces in dry conditions and are, therefore, relevant in a prebiotic context envisaging dry and wet cycles occurring, at mineral surfaces, in a small pool.

A Possible Path to Prebiotic Peptides Involving Silica and Hydroxy Acid-Mediated Amide Bond Formation.

The formation of alanine and glycine oligomers in films produced by drying aqueous mixtures of lactic acid and silica nanoparticles has been studied as a model prebiotic reaction. The addition of silica results in alanine or glycine enrichment in the polymers. Oligomerization proceeds through ester-mediated peptide bond formation in an acidic and evaporative environment at temperatures as low as 85 °C. For both amino acids, the dominant species produced in the presence of silica and lactic acid are rich in amide bonds and deficient in ester linkages. At higher temperatures, glycine and alanine oligomers contain only a single hydroxy acid residue conjugated to the peptide N terminus. Similar product distributions occur with silica particles prereacted with lactic acid, which suggests the catalytic role of a functionalized surface. This work highlights the role minerals might have served in transitioning from oligomers with both ester and amide linkages (depsipeptides) to peptides in a prebiotic context.

Proton irradiation: a key to the challenge of N-glycosidic bond formation in a prebiotic context

The formation of nucleosides in abiotic conditions is a major hurdle in origin-of-life studies. We have determined the pathway of a general reaction leading to the one-pot synthesis of ribo- and 2′-deoxy-ribonucleosides from sugars and purine nucleobases under proton irradiation in the presence of a chondrite meteorite. These conditions simulate the presumptive conditions in space or on an early Earth fluxed by slow protons from the solar wind, potentially mimicking a plausible prebiotic scenario. The reaction (i) requires neither pre-activated precursors nor intermediate purification/concentration steps, (ii) is based on a defined radical mechanism, and (iii) is characterized by stereoselectivity, regioselectivity and (poly)glycosylation. The yield is enhanced by formamide and meteorite relative to the control reaction.

The Prebiotic C-Terminal Elongation of Peptides Can Be Initiated by N-Carbamoyl Amino Acids.

The formation of peptides upon 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide (EDC)-promoted activation of N-carbamoylamino acids (CAA), was considered in the scope of our recent works on carbodiimide promoted C-terminus elongation of peptides in a prebiotic context. Thus EDC promoted activation of CAA derivatives of Tyr(Me) or Ala in dilute aqueous medium pH 5.5-6.5 in the presence of excess of AA, resulted in peptide formation by C-terminus activation/elongation. Kinetic results similar to those of EDC-mediated activation of N-acyl-AA lead us to postulate the formation of a 2-amino-5(4H)-oxazolone intermediate by cyclization of the activated CAA, in spite of the absence of epimerization occurred at CAA residues. Thus, in a prebiotic context, CAA may have played a similar role as N-acyl-AA in the initiation of C-terminus peptide elongation.

Xylonucleic acid: synthesis, structure, and orthogonal pairing properties.

There is a common interest for studying xeno-nucleic acid systems in the fields of synthetic biology and the origin of life, in particular, those with an engineered backbone and possessing novel properties. Along this line, we have investigated xylonucleic acid (XyloNA) containing a potentially prebiotic xylose sugar (a 3′-epimer of ribose) in its backbone. Herein, we report for the first time the synthesis of four XyloNA nucleotide building blocks and the assembly of XyloNA oligonucleotides containing all the natural nucleobases. A detailed investigation of pairing and structural properties of XyloNAs in comparison to DNA/RNA has been performed by thermal UV-melting, CD, and solution state NMR spectroscopic studies. XyloNA has been shown to be an orthogonal self-pairing system which adopts a slightly right-handed extended helical geometry. Our study on one hand, provides understanding for superior structure-function (-pairing) properties of DNA/RNA over XyloNA for selection as an informational polymer in the prebiotic context, while on the other hand, finds potential of XyloNA as an orthogonal genetic system for application in synthetic biology.

Non-enzymatic ribonucleotide reduction in the prebiotic context.

Model studies of prebiotic chemistry have revealed compelling routes for the formation of the building blocks of proteins and RNA, but not DNA. Today, deoxynucleotides required for the construction of DNA are produced by reduction of nucleotides catalysed by ribonucleotide reductases, which are radical enzymes. This study considers potential non-enzymatic routes via intermediate radicals for the ancient formation of deoxynucleotides. In this context, several mechanisms for ribonucleotide reduction, in a putative H2 S/HS(.) environment, are characterized using computational chemistry. A bio-inspired mechanistic cycle involving a keto intermediate and HSSH production is found to be potentially viable. An alternative pathway, proceeding through an enol intermediate is found to exhibit similar energetic requirements. Non-cyclical pathways, in which HSS(.) is generated in the final step instead of HS(.) , show a markedly increased thermodynamic driving force (ca. 70 kJ mol(-1) ) and thus warrant serious consideration in the context of the prebiotic ribonucleotide reduction.

Quasispecies in population of compositional assemblies.

BackgroundThe quasispecies model refers to information carriers that undergo self-replication with errors. A quasispecies is a steady-state population of biopolymer sequence variants generated by mutations from a master sequence. A quasispecies error threshold is a minimal replication accuracy below which the population structure breaks down. Theory and experimentation of this model often refer to biopolymers, e.g. RNA molecules or viral genomes, while its prebiotic context is often associated with an RNA world scenario. Here, we study the possibility that compositional entities which code for compositional information, intrinsically different from biopolymers coding for sequential information, could show quasispecies dynamics.ResultsWe employed a chemistry-based model, graded autocatalysis replication domain (GARD), which simulates the network dynamics within compositional molecular assemblies. In GARD, a compotype represents a population of similar assemblies that constitute a quasi-stationary state in compositional space. A compotype's center-of-mass is found to be analogous to a master sequence for a sequential quasispecies. Using single-cycle GARD dynamics, we measured the quasispecies transition matrix (Q) for the probabilities of transition from one center-of-mass Euclidean distance to another. Similarly, the quasispecies’ growth rate vector (A) was obtained. This allowed computing a steady state distribution of distances to the center of mass, as derived from the quasispecies equation. In parallel, a steady state distribution was obtained via the GARD equation kinetics. Rewardingly, a significant correlation was observed between the distributions obtained by these two methods. This was only seen for distances to the compotype center-of-mass, and not to randomly selected compositions. A similar correspondence was found when comparing the quasispecies time dependent dynamics towards steady state. Further, changing the error rate by modifying basal assembly joining rate of GARD kinetics was found to display an error catastrophe, similar to the standard quasispecies model. Additional augmentation of compositional mutations leads to the complete disappearance of the master-like composition.ConclusionsOur results show that compositional assemblies, as simulated by the GARD formalism, portray significant attributes of quasispecies dynamics. This expands the applicability of the quasispecies model beyond sequence-based entities, and potentially enhances validity of GARD as a model for prebiotic evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0265-1) contains supplementary material, which is available to authorized users.

Sunlight-initiated chemistry of aqueous pyruvic acid: building complexity in the origin of life.

Coupling chemical reactions to an energy source is a necessary step in the origin of life. Here, we utilize UV photons provided by a simulated sun to activate aqueous pyruvic acid and subsequently prompt chemical reactions mimicking some of the functions of modern metabolism. Pyruvic acid is interesting in a prebiotic context due to its prevalence in modern metabolism and its abiotic availability on early Earth. Here, pyruvic acid (CH3COCOOH, a C3 molecule) photochemically reacts to produce more complex molecules containing four or more carbon atoms. Acetoin (CH3CHOHCOCH3), a C4 molecule and a modern bacterial metabolite, is produced in this chemistry as well as lactic acid (CH3CHOHCOOH), a molecule which, when coupled with other abiotic chemical reaction pathways, can provide a regeneration pathway for pyruvic acid. This chemistry is discussed in the context of plausible environments on early Earth such as near the ocean surface and atmospheric aerosol particles. These environments allow for combination and exchange of reactants and products of other reaction environments (such as shallow hydrothermal vents). The result could be a contribution to the steady increase in chemical complexity requisite in the origin of life.

Infrared spectral investigations of UV irradiated nucleobases adsorbed on mineral surfaces

The interaction between electromagnetic radiation and bio-molecules in heterogeneous environments is a prebiotically relevant process. Minerals may have a pivotal role in the prebiotic evolution of complex chemical systems, mediating the effects of electromagnetic radiation, influencing the photostability of bio-molecules, catalyzing important chemical reactions and/or protecting molecules against degradation. In particular, nucleobases are relevant bio-molecules to investigate both in the prebiotic context, because they are coding components of nucleic acids, and from the standpoint of the survival of biological systems in space conditions. Several studies on the photodynamics of nucleobases suggest that their structure could have been naturally selected for the ability to dissipate electronic energy through ultrafast photophysical decay. Considering the putative involvement of minerals in the prebiotic chemistry, it is necessary to study the photostability of nucleobases under space conditions in the presence of mineral matrices, to investigate both the prebiotic processes that might have had a role in the development of the first living entities on Earth and the physical and chemical processes occurring in extraterrestrial environments. We focused our study on the characterization of the nature of the interaction between nucleobases and the surface of the minerals magnesium oxide and forsterite by infrared vibrational spectroscopy. We observed that most of the characteristic bands of pure nucleobases vanished when adsorbed on magnesium oxide. On the contrary, in the case of adenine and uracil adsorbed on forsterite, very intense nucleobase absorption peaks appeared. This phenomenon pertains to the surface selection rules changes related to molecular orientation. Moreover, based on the vibrational shifts, we deduced the molecular interaction sites with the mineral surfaces. Furthermore, we investigated the photostability of nucleobases adsorbed on such minerals through in situ UV irradiation experiments. Experimental results confirm the high intrinsic photostability of such molecules, because a rather low probability of interaction between UV radiation and nucleobases was estimated, and furthermore indicate that cytosine and hypoxanthine have a greater photostability compared to adenine and uracil, both pure and adsorbed onto magnesium oxide and forsterite.

Molecular alignment and chirality in gaseous streams and vortices

The discovery of collisional mechanisms, leading to aligned molecules in gaseous streams, opened the way to the research of possible origin of chiral discrimination involving aligned reactants in molecular dynamics. Experimental evidence is being provided that translational-rotational motions (such as those occurring in vortices), in the liquid phase first and in the gas phase more recently, show manifestations of chiral effects, revealing interesting relations with scenarios on the emergence of chiral selectivity. In this account, we also report the results of experiments of enantiomeric enrichment induced on chiral rotamers by rotational-translational motion. Several chiral molecules were expanded in supersonic seeded molecular beams and the vortex motion was generated by two molecular drag pumps with a right- and a left-handed screw motion, respectively. Connections can be established with many processes occurring in the Universe (and thus possibly related to a prebiotic context), like the stellar accretion of low-mass stars like the Sun and the flowing in atmospheres of rotating bodies.

On the applicability of solventless and solid-state reactions to the meteoritic chemistry

AbstractMost chemical reactions on asteroids, from which meteors and meteorites originate, are hypothesized to occur primarily in the solid mixtures. Some secondary chemical reactions may have occurred during the periods of the aqueous alteration of the asteroids. A myriad of organic compounds have been isolated from the meteorites, but the chemical conditions during which they were formed are only partially elucidated. In this paper, we propose that numerous meteoritic organic compounds were formed by the solventless and solid-state reactions that were only recently explored in conjunction with the green chemistry. A typical solventless approach exploits the phenomenon of the mixed melting points. As the solid materials are mixed together, the melting point of the mixture becomes lower than the melting points of its individual components. In some cases, the entire mixture may melt upon mixing. These reactions could then occur in a melted state. In the traditional solid-state reactions, the solids are mixed together, which allows for the intimate contact of the reactants, but the reaction occurs without melting. We have shown various examples of the known solventless and solid-state reactions that are particularly relevant to the meteoritic chemistry. We have also placed them in a prebiotic context and evaluated them for their astrobiological significance.

Toward understanding protocell mechanosensation.

Mechanosensitive (MS) channels can prevent bacterial bursting during hypo-osmotic shocks by responding to increases in lateral tension at the membrane level through an integrated and coordinated opening mechanism. Mechanical regulation in protocells could have been one of the first mechanisms to evolve in order to preserve their integrity against changing environmental conditions. How has the rich functional diversity found in present cells been created throughout evolution, and what did the primordial MS channels look like? This review has been written with the aim of identifying which factors may have been important for the appearance of the first osmotic valve in a prebiotic context, and what this valve may have been like. It highlights the mechanical properties of lipid bilayers, the association of peptides as aggregates in membranes, and the conservation of sequence motifs as central aspects to understand the evolution of proteins that gate below the tension required for spontaneous pore formation and membrane rupture. The arguments developed here apply to both MscL and MscS homologs, but could be valid to mechano-susceptible proteins in general.

From prebiotic macromolecules to synthetic polypeptides: a new, efficient synthesis of α‐amino acid N‐carboxyanhydrides (NCAs)

AbstractWhile polypeptide materials present important application potentialities, the expense of amino acid N‐carboxyanhydride (NCA) monomers strongly limits their applications. We present here a new, promising synthetic route to NCA through N‐carbamoylamino acid nitrosation by gaseous NOx(1 < x < 2) in the solid–gas phase. This very efficient reaction (which was originally developed in a prebiotic context) works in the absence of solvent and with minimum waste, and presents interesting economic features. Some mechanistic investigations aimed at the optimisation and scale‐up of this reaction in the solid‐gas phase are presented.© 2002 Society of Chemical Industry