Prebiotic Systems Research Articles

Scum of the Earth: A Hypothesis for Prebiotic Multi-Compartmentalised Environments.

Compartmentalisation by bioenergetic membranes is a universal feature of life. The eventual compartmentalisation of prebiotic systems is therefore often argued to comprise a key step during the origin of life. Compartments may have been active participants in prebiotic chemistry, concentrating and spatially organising key reactants. However, most prebiotically plausible compartments are leaky or unstable, limiting their utility. Here, we develop a new hypothesis for an origin of life environment that capitalises upon, and mitigates the limitations of, prebiotic compartments: multi-compartmentalised layers in the near surface environment—a ’scum’. Scum-type environments benefit from many of the same ensemble-based advantages as microbial biofilms. In particular, scum layers mediate diffusion with the wider environments, favouring preservation and sharing of early informational molecules, along with the selective concentration of compatible prebiotic compounds. Biofilms are among the earliest traces imprinted by life in the rock record: we contend that prebiotic equivalents of these environments deserve future experimental investigation.

Astrochemical Pathways to Complex Organic and Prebiotic Molecules: Experimental Perspectives for In Situ Solid-State Studies.

A deep understanding of the origin of life requires the physical, chemical, and biological study of prebiotic systems and the comprehension of the mechanisms underlying their evolutionary steps. In this context, great attention is paid to the class of interstellar molecules known as “Complex Organic Molecules” (COMs), considered as possible precursors of prebiotic species. Although COMs have already been detected in different astrophysical environments (such as interstellar clouds, protostars, and protoplanetary disks) and in comets, the physical–chemical mechanisms underlying their formation are not yet fully understood. In this framework, a unique contribution comes from laboratory experiments specifically designed to mimic the conditions found in space. We present a review of experimental studies on the formation and evolution of COMs in the solid state, i.e., within ices of astrophysical interest, devoting special attention to the in situ detection and analysis techniques commonly used in laboratory astrochemistry. We discuss their main strengths and weaknesses and provide a perspective view on novel techniques, which may help in overcoming the current experimental challenges.

Systems Chemistry Looking Forward

Systems Chemistry Looking Forward

Prebiotically Plausible RNA Activation Compatible with Ribozyme-Catalyzed Ligation.

RNA‐catalyzed RNA ligation is widely believed to be a key reaction for primordial biology. However, since typical chemical routes towards activating RNA substrates are incompatible with ribozyme catalysis, it remains unclear how prebiotic systems generated and sustained pools of activated building blocks needed to form increasingly larger and complex RNA. Herein, we demonstrate in situ activation of RNA substrates under reaction conditions amenable to catalysis by the hairpin ribozyme. We found that diamidophosphate (DAP) and imidazole drive the formation of 2′,3′‐cyclic phosphate RNA mono‐ and oligonucleotides from monophosphorylated precursors in frozen water‐ice. This long‐lived activation enables iterative enzymatic assembly of long RNAs. Our results provide a plausible scenario for the generation of higher‐energy substrates required to fuel ribozyme‐catalyzed RNA synthesis in the absence of a highly evolved metabolism.

Thresholds in Origin of Life Scenarios.

SummaryThresholds are widespread in origin of life scenarios, from the emergence of chirality, to the appearance of vesicles, of autocatalysis, all the way up to Darwinian evolution. Here, we analyze the “error threshold,” which poses a condition for sustaining polymer replication, and generalize the threshold approach to other properties of prebiotic systems. Thresholds provide theoretical predictions, prescribe experimental tests, and integrate interdisciplinary knowledge. The coupling between systems and their environment determines how thresholds can be crossed, leading to different categories of prebiotic transitions. Articulating multiple thresholds reveals evolutionary properties in prebiotic scenarios. Overall, thresholds indicate how to assess, revise, and compare origin of life scenarios.

The Transformation by Catalysis of Prebiotic Chemical Systems to Useful Biochemicals: A Perspective Based on IR Spectroscopy of the Primary Chemicals II. Catalysis and the Building of RNA

Having found that carbonyl sulfide (COS), works well as a catalyst in the transformation of amino acids to polypeptides, we have now tested COS as a catalyst also for the formation of substances that might be thought of as partners in the building of RNA. The model used was selective energy transfer (SET). This model implies that a certain number of vibrational quanta are donated from the catalyst system and a corresponding number of quanta of the reactant accept the energy thus transferred. In this way, we found that carbonyl sulfide, COS, was a perfect catalyst for combining, first, five molecules of formaldehyde to form one molecule of ribose, and next, five molecules of hydrogen cyanide, HCN, to form one molecule of adenine, one of the nucleobases of RNA. However, beyond this, we found that COS was a perfect catalyst for precisely all reactions, needed to build the RNA, ribonucleic acid.

The kinetics and mechanisms of reactions in the flow systems glycine-sodium trimetaphosphate-imidazoles: the crucial role of imidazoles in prebiotic peptide syntheses.

The kinetics of oligopeptides formation in the flow systems glycine-sodium trimetaphosphate-imidazole/N-methylimidazole at thermocyclic regime has been investigated by HPLC and 31P NMR methods in the ranges of temperature from 45 to 90°C and pH from 8.5 to 11.5. Detailed reaction mechanisms have been proposed and justified by quantum chemical calculations using DFT method at the CAM-B3LYP/TZVP level with accounting solvent effect by the C-PCM model. A new imidazole catalysis mechanism by which imidazole reacts with cyclic N,O-phosphoryl glycine giving N-imidazolyl-O-glycyl phosphate as a key intermediate was proposed and validated. It is emphasized that while in the absence of imidazoles, prebiotic activation of amino acids occurs at the N-terminus, in the presence of imidazoles it shifts to the O-terminus. This means that in the peptide elongation N-imidazolyl-O-aminoacyl phosphates play in prebiotic systems the outstanding role similar to that of aminoacyl adenylates formed at the ATP and aminoacyl-tRNA synthetases presence in biosystems. The new crucial role of imidazoles in prebiotic evolution has been noticed. The systems used and modes of their conversion can be good models for prebiotic peptide syntheses in a flow thermocyclic regime.

Dissipative Self-Assembly of Dynamic Multicompartmentalized Microsystems with Light-Responsive Behaviors

Summary Living cells are compartmentalized systems operating far from thermodynamic equilibrium and consume energy from the environment to carry out their functions. The construction of biomimetic synthetic compartments has both scientific and technological value. Despite many advances, the assembly of synthetic compartments that present nonequilibrium behaviors based on dissipative (or transient) self-assembly remains a grand challenge. Here, we describe the design and synthesis of multicompartmental systems with an active microstructure and complex behaviors. By including an artificial pathway for energy dissipation, we demonstrate the autonomous generation of active polymeric systems using a strategy based on polymerization-induced self-assembly (PISA), driven by chemical fuel. Remarkably, these self-organized synthetic systems exhibit a dynamic change in their multicompartmental structures when exposed to light. This work introduces a strategy toward the design and construction of synthetic compartments with a dynamic structure and also presents pathways to engineer materials with spatially controllable structures and functionalities.

The Transformation by Catalysis of Prebiotic Chemical Systems to Useful Biochemicals: A Perspective Based on IR Spectroscopy of the Primary Chemicals: I. The Synthesis of Peptides by the Condensation of Amino Acids

It is now widely speculated that life originated at the “Black Smokers” of the undersea hydrothermal vents, where conditions exist for the formation of the primary ingredients and their subsequent transformation to higher biotic species such as amino acids, alcohols, etc. Any possible routes for the prebiotic oligomerization of simple compounds like amino acids, necessary for cell formation, has so far not been well understood. However, Leman et al. recently reported that under standard laboratory conditions carbonyl sulfide (COS) can “mediate” the oligomerization of simple amino acids in moderate yield. COS being a well-known volcanic gas points to its possible role in prebiotic peptide formation in the environment of the hydrothermal vents. Based on a previously developed and tested model for selective (vibrational) energy transfer (SET), we show that a COS-catalyzed condensation of α-amino-acids can lead to the formation of polypeptides. We also indicate that other agents can act as catalysts of the amino acid condensation, such as Fe(CN)63− and cyanamide (H2N-CN). This is related to the existence of vibrations with a frequency near to that of the critical vibration of the reactant, ρw (NH2). This wagging vibration occurs at 1048 ± 10 cm−1 (the mean value of Cu and Ni complexes) and, as the vibration of the presumed catalyst lies at 2079 cm−1, one notes that one quantum of the catalyst equals two quanta of the NH2 wagging: 2079/2 × 1048 = 0.9919. This is a good indication of a resonance.

Catalyst: Can Systems Chemistry Unravel the Mysteries of the Chemical Origins of Life?

Daniela Kroiss obtained her MSc degree in biotechnology at BOKU and is currently a PhD student in the biochemistry program at CUNY, where she works on a joint project between the Nanoscience Initiative and the University of Strathclyde. Gonen Ashkenasy is head of the Laboratory for Systems Chemistry at the Ben-Gurion University Chemistry Department. His research focuses on the design and analysis of synthetic replication networks. Adam Braunschweig earned his PhD in organic chemistry at the University of California and is an associate professor in the CUNY Nanoscience Initiative. His research focuses on the interface of organic chemistry with biology and material science. Tell Tuttle obtained his PhD in theoretical chemistry at Goteborg University and is a professor of theoretical chemistry at the University of Strathclyde. His research focuses on the directed discovery of peptide-based materials. Rein Ulijn gained his PhD in physical chemistry at the University of Strathclyde and is founding director of the Nanoscience Initiative at the CUNY Advanced Science Research Center. His research focuses on nanotechnology inspired by living systems.

Investigating Prebiotic Protocells for A Comprehensive Understanding of the Origins of Life: A Prebiotic Systems Chemistry Perspective.

Protocells are supramolecular systems commonly used for numerous applications, such as the formation of self-evolvable systems, in systems chemistry and synthetic biology. Certain types of protocells imitate plausible prebiotic compartments, such as giant vesicles, that are formed with the hydration of thin films of amphiphiles. These constructs can be studied to address the emergence of life from a non-living chemical network. They are useful tools since they offer the possibility to understand the mechanisms underlying any living cellular system: Its formation, its metabolism, its replication and its evolution. Protocells allow the investigation of the synergies occurring in a web of chemical compounds. This cooperation can explain the transition between chemical (inanimate) and biological systems (living) due to the discoveries of emerging properties. The aim of this review is to provide an overview of relevant concept in prebiotic protocell research.

Soft and dispersed interface-rich aqueous systems that promote and guide chemical reactions

Although aqueous solutions are considered to be sustainable, environmentally friendly reaction media, their use is often limited by poor reactant solubility. This limitation can be overcome by converting aqueous solutions into soft, dispersed interface-rich systems such as polyelectrolyte solutions, micellar solutions, oil-in-water microemulsions or vesicle dispersions. All consist of homogeneously distributed dynamic structures that, in a fashion reminiscent of enzymes, provide local environments that are different from the bulk solution. The presence of soft, dispersed interface-rich structures leads to not only selective reaction accelerations but also changes in reaction pathways, whereby chemical reactions are guided towards desired products. Once again, the analogy to enzyme-catalysed transformations is enticing. In this Review, we illustrate the general concepts applied in such systems and illustrate them with selected examples, ranging from enzyme mimics, the preparation of conductive polymers and transition-metal-catalysed organic syntheses on the industrial scale to the chemistry of prebiotic systems. Aqueous media containing homogeneously distributed soft dynamic structures can promote a wide range of synthetic and degradative chemical reactions. This promotion is illustrated by selected examples from academia and industry, as well as from the field of prebiotic chemistry.

Reductions in ecology and thermodynamics. On the problems arising when shifting the concept of exergy to other hierarchical levels and domains

The introduction of thermodynamical views to interpret phenomenological behavior of biological systems such as organisms, populations, ecosystems or even the bio- and anthroposphere is not an easy exercise and not carried out without obstacles. The resistance against such an endeavor can be met from all scientific disciplines ranging from hardcore physics at one end to ecological fundamentalists at the other. Thus the area represents a field of tension. The reasons for this may be many, but at the center one will recognize complication that are closely linked – directly or indirectly – to the issues around philosophical reductions undertaken in the process. Such steps are necessary to take in an attempt to formulate a new holistic biological theory that tends to formulate a new metaphysics, namely that of making possible interpretations of all kinds of systems within the biosphere in terms of a thermodynamic framework. Common to all attempts have been the establishing and definition of boundaries – real, physical as well as constructed and virtual – together with a generalized application of isomorphic mathematical expressions used different sets of ontological entities that vary with levels of the biological hierarchy. Prebiotic systems represent the closest we may get to a situation where classical thermodynamic descriptions may be used but still only to a certain extent. All levels having a fixed boundary from monocellular organisms or conglomerates of such systems and upwards in the hierarchy – i.e. higher organisms and levels throughout the biological hierarchy represent systems under conditions so far away from equilibrium that they – under the given energetic, material and intrinsic constraints tend to stabilize at dynamic states or sequential semi-stable repetitive patterns. This means that we may not talk about classical thermodynamics any longer. Terms like entropy, free energy, exergy and power may be used as convenient metaphors, but it must be stated that it as a consequence is necessary to (re-)define concepts and reformulate equations based on adequate ontological units. Although they may perform with a similar phenomenology as the classical variables, it should be kept in mind that they are no longer the same, – each domain will need its own definitions.

Permeability-driven selection in a semi-empirical protocell model: the roots of prebiotic systems evolution

The origin-of-life problem has been traditionally conceived as the chemical challenge to find the type of molecule and free-solution reaction dynamics that could have started Darwinian evolution. Different autocatalytic and ‘self-replicative’ molecular species have been extensively investigated, together with plausible synthetic pathways that might have led, abiotically, to such a minimalist scenario. However, in addition to molecular kinetics or molecular evolutionary dynamics, other physical and chemical constraints (like compartmentalization, differential diffusion, selective transport, osmotic forces, energetic couplings) could have been crucial for the cohesion, functional integration, and intrinsic stability/robustness of intermediate systems between chemistry and biology. These less acknowledged mechanisms of interaction and molecular control might have made the initial pathways to prebiotic systems evolution more intricate, but were surely essential for sustaining far-from-equilibrium chemical dynamics, given their functional relevance in all modern cells. Here we explore a protocellular scenario in which some of those additional constraints/mechanisms are addressed, demonstrating their ‘system-level’ implications. In particular, an experimental study on the permeability of prebiotic vesicle membranes composed of binary lipid mixtures allows us to construct a semi-empirical model where protocells are able to reproduce and undergo an evolutionary process based on their coupling with an internal chemistry that supports lipid synthesis.

Fumarate reductase superfamily: A diverse group of enzymes whose evolution is correlated to the establishment of different metabolic pathways

Fumarate and succinate are known to be present in prebiotic systems essential for the origin of life. The fumarate and succinate interconversion reactions have been conserved throughout evolution and are found in all living organisms. The fumarate and succinate interconversion is catalyzed by the enzymes succinate dehydrogenase (SDH) and fumarate reductase (FRD).In this work we show that SDH and FRD are part of a group of enzymes that we propose to designate “fumarate reductase superfamily”. Our results demonstrate that these enzymes emerged from a common ancestor and were essential in the development of metabolic pathways involved in energy transduction.

Self-assembly of nanoparticles into biomimetic capsid-like nanoshells.

Nanoscale compartments are one of the foundational elements of living systems. Capsids, carboxysomes, exosomes, vacuoles and other nanoshells easily self-assemble from biomolecules such as lipids or proteins, but not from inorganic nanomaterials because of difficulties with the replication of spherical tiling. Here we show that stabilizer-free polydispersed inorganic nanoparticles (NPs) can spontaneously organize into porous nanoshells. The association of water-soluble CdS NPs into self-limited spherical capsules is the result of scale-modified electrostatic, dispersion and other colloidal forces. They cannot be accurately described by the Derjaguin-Landau-Vervey-Overbeek theory, whereas molecular-dynamics simulations with combined atomistic and coarse-grained description of NPs reveal the emergence of nanoshells and some of their stabilization mechanisms. Morphology of the simulated assemblies formed under different conditions matched nearly perfectly the transmission electron microscopy tomography data. This study bridges the gap between biological and inorganic self-assembling nanosystems and conceptualizes a new pathway to spontaneous compartmentalization for a wide range of inorganic NPs including those existing on prebiotic Earth.

Bringing Prebiotic Nucleosides and Nucleotides Down to Earth.

There may be more than one way leading to RNA: Recent discoveries in the synthesis of nucleoside and nucleotide precursors are described and put into the wider context of prebiotic systems chemistry. Mixing Butlerow's carbohydrate precursors with Traube's 5-formylaminopyrimidines has led to the formation of prebiotic purine nucleosides whereas the mixing of 5-phosphoribose with barbituric acid and melamine gave supramolecular fibers from stacks of Whitesides' rosettas.

Small genomes and the difficulty to define minimal translation and metabolic machineries

The notion of minimal life has sparked the interest of scientists in different fields, ranging from the origin-of-life research to biotechnology-oriented synthetic biology. Whether the interest is focused on the emergence of protocells out of prebiotic systems or the design of a cell chassis ready to incorporate new devices and functions, proposing minimal combinations of genes for life is not a trivial task. Using comparative genomics and biochemistry of endosymbionts (i.e., intracellular mutualistic symbionts) and intracellular parasites, a decade ago we proposed the core of a minimal gene set for a simple heterotrophic cell adapted to a chemically complex environment. In this work, we discuss the state-of-the-art of the definition of the minimal genome, based on our current knowledge about bacteria with naturally reduced genomes, including both endosymbionts and free-living cells. Any proposed minimal genome would be composed by a set of protein-coding and RNA genes involved in the flux of genetic information (from DNA to functional proteins) and a group of protein-coding sequences embodying a minimalist, stoichiometrically consistent metabolic network. Although the informational portion of the minimal genome is considered quasi-universal, previous proposals have not addressed the need of tRNA post-transcriptional modifications in order to perform their function. For this reason, we have focused on the essentiality of some enzymes involved in such modifications, in order to refine the set of informational genes. As for the metabolic aspect, an obvious difficulty is that there is no one minimal gene set for life but many, depending on the environment. Among cells with reduced genomes, we find a continuum of metabolic modes, from organic matter-dependent heterotrophy to the minimally demanding autotrophy. Both best-known cases of cells with small genomes, the endosymbionts and the ultra-small free-living bacteria, speak in favor of metabolic sharing as a strong force in genome reductive evolution. A hierarchy of minimal cells supported by different metabolic networks with a complexity inversely correlated with the chemical complexity of the environment can be postulated.

Mirror Symmetry Breaking by Chirality Synchronisation in Liquids and Liquid Crystals of Achiral Molecules.

Spontaneous mirror symmetry breaking is an efficient way to obtain homogeneously chiral agents, pharmaceutical ingredients and materials. It is also in the focus of the discussion around the emergence of uniform chirality in biological systems. Tremendous progress has been made by symmetry breaking during crystallisation from supercooled melts or supersaturates solutions and by self-assembly on solid surfaces and in other highly ordered structures. However, recent observations of spontaneous mirror symmetry breaking in liquids and liquid crystals indicate that it is not limited to the well-ordered solid state. Herein, progress in the understanding of a new dynamic mode of symmetry breaking, based on chirality synchronisation of transiently chiral molecules in isotropic liquids and in bicontinuous cubic, columnar, smectic and nematic liquid crystalline phases is discussed. This process leads to spontaneous deracemisation in the liquid state under thermodynamic control, giving rise to long-term stable symmetry-broken fluids, even at high temperatures. These fluids form conglomerates that are capable of extraordinary strong chirality amplification, eventually leading to homochirality and providing a new view on the discussion of emergence of uniform chirality in prebiotic systems.

Prebiotic Competition between Information Variants, With Low Error Catastrophe Risks

During competition for resources in primitive networks increased fitness of an information variant does not necessarily equate with successful elimination of its competitors. If variability is added fast to a system, speedy replacement of pre-existing and less-efficient forms of order is required as novel information variants arrive. Otherwise, the information capacity of the system fills up with information variants (an effect referred as “error catastrophe”). As the cost for managing the system’s exceeding complexity increases, the correlation between performance capabilities of information variants and their competitive success decreases, and evolution of such systems toward increased efficiency slows down. This impasse impedes the understanding of evolution in prebiotic networks. We used the simulation platform Biotic Abstract Dual Automata (BiADA) to analyze how information variants compete in a resource-limited space. We analyzed the effect of energy-related features (differences in autocatalytic efficiency, energy cost of order, energy availability, transformation rates and stability of order) on this competition. We discuss circumstances and controllers allowing primitive networks acquire novel information with minimal “error catastrophe” risks. We present a primitive mechanism for maximization of energy flux in dynamic networks. This work helps evaluate controllers of evolution in prebiotic networks and other systems where information variants compete.