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How Did It All Begin?
The Self-Assembly of Organic Molecules and the Origin of Cellular Life (2 of 4)
by David W. Deamer
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The Prebiotic Earth
Up until the discovery that microbial life can exist near submarine hydrothermal vents at temperatures above 100° C, the consensus has been that life surely began at the Earth's surface. The reasons are easily understood. It seems likely that organic compounds in the prebiotic environment would accumulate as water-soluble compounds and surface films in the early ocean. Fluctuating environments such as tide pools would then provide a mechanism for concentrating the dilute solutions, and as the concentrated mixtures of organic compounds were dried and heated, an ongoing synthesis of polymeric material would take place (Fox and Harada, 1958; Usher, 1976).
Recent advances in our understanding of the primitive Earth have forced us to rethink this assumption. For instance, the lunar cratering record suggests that the Earth was subjected to giant impacts of comets and asteroid-sized objects about the time that the first living organisms appeared. The magnitude of energy associated with such events would vaporize some or all of the early ocean, virtually sterilizing the upper portion of the Earth's surface. The origin of life on the surface could only have occurred after the last such event.
The discovery of hydrothermal vents provided an alternative site for life's origin. Shortly after their discovery Corliss et al., (1981) and Baross and Hoffman (1985) proposed vents as a potential site for the first life on the Earth. More recently, Stevens et al., (1995) reported that hydrothermal regions surprisingly deep in the Earth's crust also have extensive microbial populations. Both hydrothermal vents and deep geothermal regions may have provided a refuge from giant impacts that sterilized the surface of the early Earth. This idea is supported by evidence from ribosomal RNA sequences which strongly suggests that the last common ancestor of all life on Earth was likely to have been a thermophilic microorganism (Woese, 1987; Pace, 1991).
A third alternative site was proposed by Bada et al., (1994) who noted that current models of solar evolution predict a young sun 20–30% less luminous than today's sun. Unless there was significant greenhouse warming, the early oceans would freeze to form an ice sheet that would be periodically thawed by impact events. It is well known that organic compounds such as amino acids have finite lifetimes in solution, and their stability decreases markedly as the temperature increases. At the highest temperatures associated with hydrothermal vents, amino acids cannot survive at all (Bada et al., 1994). A global ice cover and colder temperatures would afford significant protection against thermal degradation. It also seems likely that the concentrated mixture of solutes available during thaws could undergo a burst of chemical reactions leading to more complex molecules, a few of which could be on the evolutionary pathway to life.
To summarize, three alternative sites have now been proposed for the accumulation of organic compounds pertinent to the origin of life. Two of the alternatives place the site at the Earth's surface, the main variable being the temperature of the site. The third alternative places the site at a subsurface region associated with relatively high temperatures. The surface sites have access to light energy, chemical energy and to concentrating mechanisms, while the subsurface site has access to chemical energy in the form of certain mineral surfaces (pyrite and clays), dissolved gases like hydrogen and methane, and solutes such as ferrous iron.
The three alternatives do not represent hypotheses per se, but are more in the form of conjectures. That is, they can never be tested by direct experiment, because the origin of life occurred in an unknown environment over 3.5 billion years ago in conditions that cannot be reproduced with certainty today.
How did organic compounds appear on the early Earth?
The classic experiments of Miller (1953) showed that impressive yields of certain amino acids can be obtained when a mixture of gases (hydrogen, methane, ammonia and water vapor) is exposed to an electrical discharge. This discovery represented a major breakthrough, since amino acids are the monomers that compose all proteins. The mixture was assumed to be a simulation of the original terrestrial atmosphere which, by analogy with the outer planets, would have contained hydrogen, methane, ammonia and water vapor. At sufficiently high energy fluxes, such reducing systems of gases generate hydrogen cyanide (HCN) and formaldehyde (HCHO), which in turn react to produce amino acids. Cyanide and formaldehyde are now considered to be key reactants in simulations of prebiotic chemical pathways (Ferris and Hagan, 1984).
The possibility that organic material could readily be synthesized in prebiotic conditions was supported when it was discovered that carbonaceous meteorites also contained amino acids, hydrocarbons, and even traces of purines, one of the basic components of nucleic acids (Kvenvolden et al., 1970). If carbonaceous meteorites represent samples of the primitive solar system, it is reasonable to assume that similar synthetic chemical reactions may have occurred on the Earth's surface. With organic monomers available in reasonable concentrations on a global scale, it was not difficult to imagine that self-assembling systems of polymerized macromolecules would at some point assume the properties of the living state: the ability to exist as a membrane bounded entity, or cell, the capacity to use energy and nutrients to grow by directed polymerization processes, and the ability to divide in some way to produce another generation.
However, more recent results indicate that the early atmosphere was composed of carbon dioxide and nitrogen rather than a mixture of reduced gases (Holland, 1984; Kasting and Ackerman, 1986). Carbon dioxide does not support the rich array of synthetic pathways leading to possible monomers, and alternative sources of organic material are being considered. One possibility is that extraterrestrial infall in the form of comets and meteorites provided significant amounts of organic carbon to the Earth's surface (Oro, 1961; Anders, 1989; Chyba and Sagan, 1992).
An extraterrestrial source of organic compounds is surprising, but there is no doubt that all of the biogenic elements on the Earth (carbon, hydrogen, oxygen, nitrogen, phosphorus and sulfur) had an extraterrestrial origin simply because they were delivered by the Earth's accretion process. The question is how much chemical processing occurred before the elements were incorporated into primitive forms of life. Most likely both synthesis and infall were involved to some degree. For instance, amino acids are present only in trace amounts in carbonaceous meteorites, and furthermore are relatively unstable in water. It follows that amino acids and other water soluble organic compounds probably were synthesized continuously at the Earth's surface. On the other hand, hydrocarbon derivatives are relatively stable and compose several percent of the mass of carbonaceous meteorites, yet are not major products of Miller-Urey type reactions. It may be that hydrocarbons required by early life were primarily delivered with meteoritic infall, rather that being synthesized by terrestrial chemistry.
Estimates of accumulated organic compounds during a hundred million year late accretion period ending around 3.9 billion years ago are in the range of 1016–1018 kgs. This is less than the total organic carbon stored as oil shales, coal and other fossil deposits on the Earth (1021 kg) which represents carbon dioxide reduced to organic compounds by photosynthetic processes. On the other hand, it is several orders of magnitude greater than the organic carbon now in the biosphere, estimated to be 6 X 1014 kg. To put this value into perspective, if 6 X 1014 kg of the organic substances in the total biomass today were spread over the entire surface of the Earth, including the oceans, it would form a layer about 1 mm thick. For comparison, the amount of organic substances delivered by infall would form a layer ranging from 1.6 cm to 1.6 m thick. Although this amount of material would represent a significant source of organic carbon in the prebiotic environment if it all survived and accumulated, most of the cometary and meteoritic infall surviving atmospheric entry would presumably fall into oceans. A major fraction of the organic content would be buried as sediment, and a smaller fraction would be released into the marine environment over long time intervals. Water soluble compounds would dissolve to form a very dilute solution of organic solutes, while longer chain hydrocarbons and their derivatives would accumulate at the ocean surface to form a thin film at the air-water interface. Such films would likely become concentrated at intertidal zones by the same mechanism that forms sea foam from active organic compounds today. It follows that probable sites for the physical and chemical processes leading to the origin of living cells would be tide pools or geothermal region in which hydrocarbon derivatives accumulated and were mixed with water-soluble organics during cyclic drying and rehydration processes.
Self-assembly processes: soap bubbles and membranes
All life today has units that we call cells. Did life arise from pre-existing cellular structures, or did cellular life develop only at a later evolutionary stage? As noted earlier, there were no large molecules like nucleic acids and proteins available on the prebiotic Earth to direct the assembly processes characteristic of life, so the first forms of life must have arisen through self-assembly processes. Familiar examples of such processes today include the formation of bubbles from soap molecules, or the foam that accumulates in tide pools. The main point to be made in this section is that certain kinds of organic compounds called amphiphilic molecules are able to self-assemble into microscopic bubble-like structures. Such structures form spontaneously, and perhaps provided the original membrane-bounded environment required for cellular life to begin.
We will first outline the biophysical principles that govern self-assembly processes and indicate how they can be used to investigate the origin of cellular systems.
1. Bilayers assemble from of variety of amphiphilic compounds
Although contemporary cell membranes incorporate phospholipids as the primary component of the bilayer, it is not necessary to think that such complex molecules were required for early cellular life. In fact, simpler amphiphilic molecules can also assemble into bilayer membranes, even single-chain amphiphiles such as soap molecules. It seems likely that primitive cells incorporated lipid-like molecules from the environment as a nutrient, rather than undertaking the much more complex process of synthesizing complex lipids by an enzyme-catalyzed process.
2. Bilayer permeability strongly depends on chain length of the amphiphilic molecules
We tend to think of the lipid bilayer as being a nearly impenetrable barrier to ionic solutes such as salt (sodium chloride) and other large, polar molecules like amino acids. But then how did early cellular life function in the absence of highly evolved transport enzymes that translocate ionic nutrients and metabolites across the bilayer barrier? It is true that lipid bilayers of contemporary cell membranes present a significant permeability barrier that is necessary for normal cell functions, particularly those related to bioenergetics of ion transport and chemiosmotic ATP synthesis. However, recent results show that shortening lipid chain length from 18 to 14 carbons increases the permeation of ionic solutes by several orders of magnitude. This level of permeability is sufficient to encapsulate large molecules such as proteins and polynucleotides, yet still allow external substrate to reach an encapsulated enzyme. It follows that early cell membranes could have been composed of shorter chain lipids that provided access to nutrients for macromolecules undergoing growth and replication in an encapsulated microenvironment.
3. Macromolecules can be encapsulated in bilayer vesicles under simulated prebiotic conditions
A third conceptual problem has been to imagine how lipid bilayers could capture macromolecules in the first place, given that the bilayer must present a nearly impenetrable barrier if the macromolecules are to be maintained within the membrane bounded volume. We will describe how a mixture of lipid and protein or nucleic acids can undergo drying and wetting cycles that simulate tide pools. Under these conditions, the macromolecules are readily captured in membrane-bounded vesicles.
4. Lipid bilayers grow by addition of amphiphilic compounds present in the environment
It is not sufficient for a primitive cell to replicate its macromolecular components unless the boundary membrane can increase in area to accommodate the internal growth. Recent experimental results from liposome model systems demonstrate that such growth through addition of amphiphilic molecules can in fact occur.
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