The TNA-Family of Nucleic Acid Systems: Properties and Prospects

This report summarizes the content of the author's lecture given at the 9th ISSOL Conference on the 'Origin of Life' in Oaxaca on 2 July 2002*. The report consists of introductory remarks followed by a reproduction of the authentic sequence of slides shown during the lecture. Each slide figure is accompanied with a short commentary on the figure's content. The lecture dealt with the structure and the properties of TNA (alpha-threofuranosyl nucleic acid) and included results of some more recent chemical investigations that had been inspired by the simplicity of TNA's molecular architecture.     

Life on Mars: chemical arguments and clues from Martian meteorites

Primitive terrestrial life – defined as a chemical system able to transfer its molecular information via self-replication and to evolve – probably originated from the evolution of reduced organic molecules in liquid water. Several sources have been proposed for the prebiotic organic molecules: terrestrial primitive atmosphere (methane or carbon dioxide), deep-sea hydrothermal systems, and extraterrestrial meteoritic and cometary dust grains. The study of carbonaceous chondrites, which contain up to 5% by weight of organic matter, has allowed close examination of the delivery of extraterrestrial organic material. Eight proteinaceous amino acids have been identified in the Murchison meteorite among more than 70 amino acids. Engel reported that l-alanine was surprisingly more abundant than d-alanine in the Murchison meteorite. Cronin also found excesses of l-enantiomers for nonprotein amino acids. A large collection of micrometeorites has been recently extracted from Antarctic old blue ice. In the 50- to 100-μm size range, carbonaceous micrometeorites represent 80% of the samples and contain 2% of carbon, on average. They might have brought more carbon than that involved in the present surficial biomass. The early histories of Mars and Earth clearly show similarities. Liquid water was once stable on the surface of Mars, attesting the presence of an atmosphere capable of deccelerating C-rich micrometeorites. Therefore, primitive life may have developed on Mars as well and fossilized microorganisms may still be present in the near subsurface. The Viking missions to Mars in 1976 did not find evidence of either contemporary or past life, but the mass spectrometer on the lander aeroshell determined the atmospheric composition, which has allowed a family of meteorites to be identified as Martian. Although these samples are essentially volcanic in origin, it has been recognized that some of them contain carbonate inclusions and even veins that have a carbon isotopic composition indicative of an origin from Martian atmospheric carbon dioxide. The oxygen isotopic composition of these carbonate deposits allows calculation of the temperature regime existing during formation from a fluid that dissolved the carbon dioxide. As the composition of the fluid is unknown, only a temperature range can be estimated, but this falls between 0° and 90°C, which would seem entirely appropriate for life processes. It was such carbonate veins that were found to host putative microfossils. Irrespective of the existence of features that could be considered to be fossils, carbonate-rich portions of Martian meteorites tend to have material, at more than 1000 ppm, that combusts at a low temperature; i.e., it is an organic form of carbon. Unfortunately, this organic matter does not have a diagnostic isotopic signature so it cannot be unambiguously said to be indigenous to the samples. However, many circumstantial arguments can be made to the effect that it is cogenetic with the carbonate and hence Martian. If it could be proved that the organic matter was preterrestrial, then the isotopic fractionation between it and the carbon is in the right sense for a biological origin. Received: January 22, 1998 / Accepted: February 16, 1998     

Asymmetric Spatiotemporal Evolution of Prebiotic Homochirality

The role of asymmetry on the evolution of prebiotic homochirality is investigated in the context of autocatalytic polymerization reaction networks. A model featuring enantiometric cross-inhibition and chiral bias is used to study the diffusion equations controlling the spatiotemporal development of left and right-handed domains. Bounds on the chiral bias are obtained based on present-day constraints on the emergence of life on early Earth. The viability of biasing mechanisms such as weak neutral currents and circularly polarized UV light is discussed. The results can be applied to any hypothetical planetary platform.     

Looking for the Primordial Genetic Honeycomb

All life forms on Earth share the same biological program based on the DNA/RNA genomes and proteins. The genetic information, recorded in the nucleotide sequence of the DNA and RNA molecule, supplies the language of life which is transferred through the different generations, thus ensuring the perpetuation of genetic information on Earth. The presence of a genetic system is absolutely essential to life. Thus, the appearance in an ancestral era of a nucleic acid-like polymer able to undergo Darwinian evolution indicates the beginning of life on our planet. The building of primordial genetic molecules, whatever they were, required the presence of a protected environment, allowing the synthesis and concentration of precursors (nucleotides), their joining into larger molecules (polynucleotides), the protection of forming polymers against degradation (i.e. by cosmic and UV radiation), thus ensuring their persistence in a changing environment, and the expression of the “biological” potential of the molecule (its capacity to self-replicate and evolve). Determining how these steps occurred and how the primordial genetic molecules originated on Earth is a very difficult problem that still must be resolved. It has long been proposed that surface chemistry, i.e. on clay minerals, could have played a crucial role in the prebiotic formation of molecules basic to life. In the present work, we discuss results obtained in different fields that strengthen the hypothesis of a clay-surface-mediated origin of genetic material. Presented at: National Workshop on Astrobiology: Search for Life in the Solar System, Capri, Italy, 26 to 28 October, 2005.     

Analysis of Evolutionarily Independent Protein-RNA Complexes Yields a Criterion to Evaluate the Relevance of Prebiotic Scenarios

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Reduction and Activation of Phosphate on the Primitive Earth

Electrical discharges in water-saturated N₂ containing 1–10% CH₄ were shown earlier toreduce phosphate to phosphite. This mechanism was suggestedas a possible source of water-soluble phosphorus-containing compounds in volcanic environments on the prebiotic Earth.We have now extended our investigations to gas mixtures inwhich CO₂ and N₂ are the main components, and studied the effect of introducing smallamounts of H₂ and CO.We show that surprisingly high conversions to phosphite occurin reducing mixtures and thatseveral percent reduction of apatite occurs even in thepresence of as little as 1% each of H₂ and CO. We were also able to confirm a previous report ofpolyphosphate production as a result of heating the mineral apatite in the presence of other minerals.     

Thermal Energy and the Origin of Life

Life has evolved on Earth with electromagnetic radiation (light), fermentable organic molecules, and oxidizable chemicals as sources of energy. Biological use of thermal energy has not been observed although heat, and the thermal gradients required to convert it into free energy, are ubiquitous and were even more abundant at the time of the origin of life on Earth. Nevertheless, Earth-organisms sense thermal energy, and in suitable environments may have gained the capability to use it as energy source. It has been proposed that the first organisms obtained their energy by a first protein named pF₁ that worked on a thermal variation of the binding change mechanism of today's ATP sythase enzyme. Organisms using thermosynthesis may still live where light or chemical energy sources are not available. Possible suitable examples are subsurface environments on Earth and in the outer Solar System, in particular the subsurface oceans of the icy satellites of Jupiter and Saturn.     

Growth of Organic Microspherules in Sugar-Ammonia Reactions

Reaction of small sugars of less than four carbons with ammonia in water yielded organic microspherules generally less than ten microns in size. The time course of microspherule growth was examined for the D-erythrose-ammonia reaction that yielded microspherules attached to the glass walls of containers. Measurements were made of the elemental composition and infrared spectrum of the microspherule material. These viscose semi-solid microspherules are viewed as possible containers for prebiotic catalytic processes relevant to the origin of life.     

The Sugar Model: Autocatalytic Activity of the Triose–Ammonia Reaction

Reaction of triose sugars with ammonia under anaerobic conditions yielded autocatalytic products. The autocatalytic behavior of the products was examined by measuring the effect of the crude triose–ammonia reaction product on the kinetics of a second identical triose–ammonia reaction. The reaction product showed autocatalytic activity by increasing both the rate of disappearance of triose and the rate of formation of pyruvaldehyde, the product of triose dehydration. This synthetic process is considered a reasonable model of origin-of-life chemistry because it uses plausible prebiotic substrates, and resembles modern biosynthesis by employing the energized carbon groups of sugars to drive the synthesis of autocatalytic molecules.     

Microbial life in glacial ice and implications for a cold origin of life

Application of physical and chemical concepts, complemented by studies of prokaryotes in ice cores and permafrost, has led to the present understanding of how microorganisms can metabolize at subfreezing temperatures on Earth and possibly on Mars and other cold planetary bodies. The habitats for life at subfreezing temperatures benefit from two unusual properties of ice. First, almost all ionic impurities are insoluble in the crystal structure of ice, which leads to a network of micron-diameter veins in which microorganisms may utilize ions for metabolism. Second, ice in contact with mineral surfaces develops a nanometre-thick film of unfrozen water that provides a second habitat that may allow microorganisms to extract energy from redox reactions with ions in the water film or ions in the mineral structure. On the early Earth and on icy planets, prebiotic molecules in veins in ice may have polymerized to RNA and polypeptides by virtue of the low water activity and high rate of encounter with each other in nearly one-dimensional trajectories in the veins. Prebiotic molecules may also have utilized grain surfaces to increase the rate of encounter and to exploit other physicochemical features of the surfaces.     

The Lipid World

The continuity of abiotically formed bilayer membraneswith similar structures in contemporary cellular life,and the requirement for microenvironments in whichlarge and small molecules could be compartmentalized, support the idea that amphiphilic boundary structurescontributed to the emergence of life. As an extensionof this notion, we propose here a `Lipid World'scenario as an early evolutionary step in theemergence of cellular life on Earth. This conceptcombines the potential chemical activities of lipidsand other amphiphiles, with their capacity to undergospontaneous self-organization into supramolecularstructures such as micelles and bilayers. Inparticular, the documented chemical rate enhancementswithin lipid assemblies suggest that energy-dependentsynthetic reactions could lead to the growth andincreased abundance of certain amphiphilic assemblies.We further propose that selective processes might acton such assemblies, as suggested by our computersimulations of mutual catalysis among amphiphiles. Asdemonstrated also by other researchers, such mutualcatalysis within random molecular assemblies couldhave led to a primordial homeostatic system displayingrudimentary life-like properties. Taken together,these concepts provide a theoretical framework, andsuggest experimental tests for a Lipid World model forthe origin of life.     

The Sugar Model: Catalytic Flow Reactor Dynamics of Pyruvaldehyde Synthesis from Triose Catalyzed by Poly-L-Lysine Contained in a Dialyzer

The formation of pyruvaldehyde from triose sugars was catalyzedby poly-L-lysine contained in a small dialyzer with a 100molecular weight cut off (100 MWCO) suspended in a much largertriose substrate reservoir at pH 5.5 and 40 °C. Thepolylysine confined in the dialyzer functioned as a catalyticflow reactor that constantly brought in triose from thesubstrate reservoir by diffusion to offset the drop in trioseconcentration within the reactor caused by its conversion topyruvaldehyde. The catalytic polylysine solution (400 mM, 0.35mL) within the dialyzer generated pyruvaldehyde with a syntheticintensity (rate/volume) that was 3400 times greater than that ofthe triose substrate solution (12 mM, 120 mL) outside thedialyzer. Under the given conditions the final yield ofpyruvaldehyde was greater than twice the weight of thepolylysine catalyst. During the reaction the polylysine catalystwas poisoned presumably by reaction of its amino groups withaldehyde reactants and products. Similar results were obtainedusing a dialyzer with a 500 MWCO. The dialyzer method ofcatalyst containment was selected because it provides a simpleand easily manipulated experimental system forstudying the dynamics and evolutionary development of confinedautocatalytic processes related to the origin of life underanaerobic conditions.     

Formation of Peptide Bonds from Metastable versus Crystalline Phase: Implications for the Origin of Life

Formation of peptide bonds was attempted bythermal activation of dry amino acids from aqueous solutionthat simulated prebiotic evaporative environments. Theevaporation trend of amino acids solutions shows abifurcation and can lead to either a crystalline phase(near equilibrium) or a metastable non-crystalline phase(far from equilibrium). Only amino acids in this metastablephase are able to form peptide bonds by thermal activationat temperatures that are generated by solar radiationtoday. We suggest that this metastable phase is the idealinitial material to trigger amino acid assemblage withprotein-like structure because provide the driving force(supersaturation) for an intense interaction betweenmonomers of different amino acids and allows activation ofthese monomers in plausible prebiotic conditions.     

Sites for Phosphates and Iron-Sulfur Thiolates in the First Membranes: 3 to 6 Residue Anion-Binding Motifs (Nests)

Nests are common three to six amino acid residue motifs in proteins where successive main chain NH groups bind anionic atoms or groups. On average 8% of residues in proteins belong to nests. Nests form a key part of a number of phosphate binding sites, notably the P-loop, which is the commonest of the binding sites for the phosphates of ATP and GTP. They also occur regularly in sites that bind [Fe₂S₂](RS)₄ [Fe₃S₄](RS)₃ and [Fe₄S₄](RS)₄ iron-sulfur centers, which are also anionic groups. Both phosphates and iron-sulfur complexes would have occurred in the precipitates within hydrothermal vents of moderate temperature as key components of the earliest metabolism and it is likely existing organisms emerging in this milieu would have benefited from evolving molecules binding such anions. The nest conformation is favored by high proportions of glycine residues and there is evidence for glycine being the commonest amino acid during the stage of evolution when proteins were evolving so it is likely nests would have been common features in peptides occupying the membranes at the dawn of life.     

Phosphoryl amino acids: Common origin for nucleic acids and protein

A series of compounds (DAP-AA) composed of an amino acid (AA) and a dialkyl phosphoryl group (DAP) is the basic elements of life chemistry. Self-catalysis of DAP-AA gives the self-assembly oligopeptides, even in aqueous medium at 38°C. The oligo-nucleotides could also be assembled from nucleosides' phosphorylation by DAP-AA. DAP-AA acts as the energy source as well as the phosphoryl donor for the synthesis of nuclic Acids and protein. A general expression for the self assembly system is proposed.     

Smectite clays in Mars soil: Evidence for their presence and role in Viking biology experimental results

Summary Various chemical, physical and geological observations indicate that smectite clays are probably the major components of the Martian soil. Satisfactory ground-based chemical simulation of the Viking biology experimental results was obtained with the smectite clays nontronite and montmorillonite when they contained iron and hydrogen as adsorbed ions. Radioactive gas was released from the medium solution used in the Viking Labeled Release (LR) experiment when interacted with the clays, at rates and quantities similar to those measured by Viking on Mars. Heating of the active clay (mixed with soluble salts) to 160°C in CO₂ atmosphere reduced the decomposition activity considerably, again, as was observed on Mars. The decomposition reaction in LR experiment is postulated to be iron-catalyzed formate decomposition on the clay surface. The main features of the Viking Pyrolytic Release (PR) experiment were also simulated recently (Hubbard, 1979) which the iron clays, including a relatively low 1st peak and significant 2nd peak.The accumulated observations on various Martian soil properties and the results of simulation experiments, thus indicate that smectite clays are major and active components of the Martian soil. It now appears that many of the results of the Viking biology experiments can be explained on the basis of their surface activity in catalysis and adsorption.     

Thermal Wet Decomposition of Prussian Blue: Implications for Prebiotic Chemistry

The complex salt named Prussian Blue, Fe₄[Fe(CN)₆]₃?15 H₂O, can release cyanide at pH>10. From the point of view of the origin of life, this fact is of interest, since the oligomers of HCN, formed in the presence of ammonium or amines, leads to a variety of biomolecules. In this work, for the first time, the thermal wet decomposition of Prussian Blue was studied. To establish the influence of temperature and reaction time on the ability of Prussian Blue to release cyanide and to subsequently generate other compounds, suspensions of Prussian Blue were heated at temperatures from room temperature to 150° at pH 12 in NH₃ environment for several days. The NH₃ wet decomposition of Prussian Blue generated hematite, α‐Fe₂O₃, the soluble complex salt (NH₄)₄[Fe(CN₆)]?1.5 H₂O, and several organic compounds, the nature and yield of which depend on the experimental conditions. Urea, lactic acid, 5,5‐dimethylhydantoin, and several amino acids and carboxylic acids were identified by their trimethylsilyl (TMS) derivatives. HCN, cyanogen (C₂N₂), and formamide (HCONH₂) were detected in the gas phase by GC/MS analysis.     

Enantiomeric Crystallization from DL-Aspartic and DL-Glutamic Acids: Implications for Biomolecular Chirality in the Origin of Life

Amino acids in living systems consist almost exclusively of the L-enantiomer. How and when this homochiral characteristic of life came to be has been a matter of intense investigation for many years. Among the hypotheses proposed to explain theappearance of chiral homogeneity, the spontaneous resolution of conglomerates seems one of the most plausible. Racemic solids may crystallize from solution either as racemic compounds(both enantiomeric molecules in the same crystal), or lesscommonly as conglomerates (each enantiomer molecule separate indifferent enantiomeric crystals). Only conglomerates can developa spontaneous resolution (one of the enantiomeric molecule crystallizes preferentially, the other one remains in solution).Most of natural amino acids are racemic compounds at moderatetemperatures. How can we expect a hypothetical spontaneous resolution of these amino acids if they are not conglomerates?In this paper we show how DL-aspartic and DL-glutamic amino acids(racemic compounds), crystallize at ambient conditions as trueconglomerates. The experimental conditions here described,that allows this `anomalous' behaviour, could be also found innatural sedimentary environments. We suggest that these experimental procedures and its natural equivalents, have apotential interest for the investigation of the spontaneous resolution of racemic compounds comprising molecules associatedwith the origin of life.     

An Extended Model for the Evolution of Prebiotic Homochirality: A Bottom-Up Approach to the Origin of Life

A generalized autocatalytic model for chiral polymerization is investigated in detail. Apart from enantiomeric cross-inhibition, the model allows for the autogenic (non-catalytic) formation of left and right-handed monomers from a substrate with reaction rates epsilon L and epsilon R, respectively. The spatiotemporal evolution of the net chiral asymmetry is studied for models with several values of the maximum polymer length, N. For N = 2, we study the validity of the adiabatic approximation often cited in the literature. We show that the approximation obtains the correct equilibrium values of the net chirality, but fails to reproduce the short time behavior. We show also that the autogenic term in the full N = 2 model behaves as a control parameter in a chiral symmetry-breaking phase transition leading to full homochirality from racemic initial conditions. We study the dynamics of the N--> infinity model with symmetric (epsilon L = epsilon R) autogenic formation, showing that it only achieves homochirality for epsilon > epsilon c, where epsilon c is an N-dependent critical value. For epsilon 相似文献   

A theory for the origin of a self-replicating chemical system. I: Natural selection of the autogen from short,random oligomers

Summary A theory is described for the origin of a simple chemical system named an autogen, consisting of two short oligonucleotide sequences coding for two simple catalytic peptides. If the theory is valid, under appropriate conditions the autogen would be capable of self-reproduction in a truly genetic process involving both replication and translation. Limited catalytic ability, short oligomer sequences, and low selectivities leading to sloppy information transfer processes are shown to be adequate for the origin of the autogen from random background oligomers. A series of discrete steps, each highly probable if certain minimum requirements and boundary conditions are satisfied, lead to exponential increase in population of all components in the system due to autocatalysis and hypercyclic organization. Nucleation of the components and exponential increase to macroscopic amounts could occur in times on the order of weeks. The feasibility of the theory depends on a number of factors, including the capability of simple protoenzymes to provide moderate enhancements of the accuracies of replication and translation and the likelihood of finding an environment where all of the required processes can occur simultaneously. Regardless of whether or not the specific form proposed for the autogen proves to be feasible, the theory suggests that the first self-replicating chemical systems may have been extremely simple, and that the period of time required for chemical evolution prior to Darwinian natural selection may have been far shorter than generally assumed. Due to the short time required, this theory, unlike others on the origin of genetic processes, is potentially capable of direct experimental verification. A number of prerequisites leading up to such an experiment are suggested, and some have been fulfilled. If successful, such an experiment would be the first laboratory demonstration of the spontaneous emergence by natural selection of a genetic, self-replicating, and evolving molecular system, and might represent the first step in the prebiotic environment of true Darwinian evolution toward a living cell.