Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: implications for a prebiotic aqueous medium

A commonly accepted view is that life began in a marine environment, which would imply the presence of inorganic ions such as Na+, Cl-, Mg2+, Ca2+, and Fe2+. We have investigated two processes relevant to the origin of life--membrane self-assembly and RNA polymerization--and established that both are adversely affected by ionic solute concentrations much lower than those of contemporary oceans. In particular, monocarboxylic acid vesicles, which are plausible models of primitive membrane systems, are completely disrupted by low concentrations of divalent cations, such as magnesium and calcium, and by high sodium chloride concentrations as well. Similarly, a nonenzymatic, nontemplated polymerization of activated RNA monomers in ice/eutectic phases (in a solution of low initial ionic strength) yields oligomers with > 80% of the original monomers incorporated, but polymerization in initially higher ionic strength aqueous solutions is markedly inhibited. These observations suggest that cellular life may not have begun in a marine environment because the abundance of ionic inorganic solutes would have significantly inhibited the chemical and physical processes that lead to self-assembly of more complex molecular systems.     

The first cell membranes

Organic compounds are synthesized in the interstellar medium and can be delivered to planetary surfaces such as the early Earth, where they mix with endogenous species. Some of these compounds are amphiphilic, having polar and nonpolar groups on the same molecule. Amphiphilic compounds spontaneously self-assemble into more complex structures such as bimolecular layers, which in turn form closed membranous vesicles. The first forms of cellular life required self-assembled membranes that were likely to have been produced from amphiphilic compounds on the prebiotic Earth. Laboratory simulations show that such vesicles readily encapsulate functional macromolecules, including nucleic acids and polymerases. The goal of future investigations will be to fabricate artificial cells as models of the origin of life.     

The NASA Astrobiology Roadmap

The NASA Astrobiology Roadmap provides guidance for research and technology development across the NASA enterprises that encompass the space, Earth, and biological sciences. The ongoing development of astrobiology roadmaps embodies the contributions of diverse scientists and technologists from government, universities, and private institutions. The Roadmap addresses three basic questions: How does life begin and evolve, does life exist elsewhere in the universe, and what is the future of life on Earth and beyond? Seven Science Goals outline the following key domains of investigation: understanding the nature and distribution of habitable environments in the universe, exploring for habitable environments and life in our own solar system, understanding the emergence of life, determining how early life on Earth interacted and evolved with its changing environment, understanding the evolutionary mechanisms and environmental limits of life, determining the principles that will shape life in the future, and recognizing signatures of life on other worlds and on early Earth. For each of these goals, Science Objectives outline more specific high-priority efforts for the next 3-5 years. These 18 objectives are being integrated with NASA strategic planning.     

Eutectic phases in ice facilitate nonenzymatic nucleic acid synthesis

Polymeric compounds similar to oligonucleotides are relevant to the origin of life and particularly to the concept of an RNA world. Although short oligomers of RNA can be synthesized nonenzymatically under laboratory conditions by second-order reactions in concentrated solutions, there is no consensus on how these polymers could have been synthesized de novo on the early Earth from dilute solutions of monomers. To address this question in the context of an RNA world, we have explored ice eutectic phases as a reaction medium. When an aqueous solution freezes, the solutes become concentrated in the spaces between the ice crystals. The increased concentration offsets the effect of the lower temperature and accelerates the reaction. Here we show that in the presence of metal ions in dilute solutions, frozen samples of phosphoimidazolide-activated uridine react within days at -18 degrees C to form oligouridylates up to 11 bases long. Product yields typically exceed 90%, and approximately 30% of the oligomers include one or more 3'-5' linkages. These conditions facilitate not only the notoriously difficult oligouridylate synthesis, but also the oligomerization of activated cytidylate, adenylate, and guanylate. To our knowledge, this represents the first report to indicate that ice matrices on the early Earth may have accelerated certain prebiotic polymerization reactions.     

Polycyclic aromatic hydrocarbons: primitive pigment systems in the prebiotic environment.

Polycyclic aromatic hydrocarbons (PAH) in the form of polymerized derivatives represent over 90% of the organic material of carbonaceous chondrites. It now appears likely that there was substantial survival of the organic content of meteoritic and cometary infall during late accretion, so that PAH would presumably be major components of the organic inventory present on the prebiotic Earth. An important question relative to chemical evolution and energy transduction is the nature of pigments which could be available to make light energy available to the earliest cellular forms of life. PAH and their derivatives all absorb light in the near UV and blue wavelengths, and are candidates for primitive pigments. We have explored this possibility in a model system consisting of mixtures of pyrene, fluoranthene and pyrene derivatives with hexadecane, dispersed in dilute salt solutions. Upon illumination, photochemical oxidation of the hexadecane occurs, with long-chain amphiphiles such as 2-hexadecanone and 2-hexadecanol as products. Because the reaction proceeds under strictly anaerobic conditions, the source of oxygen is apparently water. We also observed acid pH shifts during illumination. Photochemical production of hydrogen ion is significant, in that chemiosmotic proton gradients across membranes are used by all contemporary cells as a source of energy for ATP synthesis and nutrient transport. To test whether the protons could be used to transduce light energy into a useful form, PAH derivatives were included in lipid bilayer membranes (liposomes). Upon illumination, protons (or acidic products) were produced and accumulated inside the vesicles, so that substantial pH gradients were established across the membranes, acid inside. We conclude that PAH dissolved in aliphatic hydrocarbons absorb light energy and use it to oxidize the hydrocarbon to long-chain amphiphilic molecules. The oxidation is accompanied by release of protons. If PAH derivatives are included in the bilayer membrane of lipid vesicles, protons accumulate within the membrane-bounded volumes to form proton gradients. This system provides a useful model of a primitive photochemical reaction in which light energy is transduced into potentially useable forms.