SELF-ASSEMBLY PROCESSES: STEPS TOWARD LIFE'S ORIGINS

David W. Deamer

Department of Chemistry and Biochemistry

University of California, Santa Cruz

Abstract

A fundamental property of life is the capacity for polymer synthesis in a confined space, using free energy and nutrients available in the environment. In contemporary cellular life, two polymers are central to this process: Nucleic acids store and express genetic information, and proteins have structural and catalytic functions. In order to have the capacity for evolution, the two polymers are necessarily linked through a genetic code and translation process that couples mutational changes to catalytic function. The origin of cellular life presumably occurred by self-assembly of organic compounds on the prebiotic Earth into encapsulated molecular systems capable of catalyzed polymer synthesis. Although it is unlikely that nucleic acids and proteins as such were components of the first living systems, analogous polymers were produced by an as yet unknown synthetic pathway, which were capable of interacting in such a way that evolution was possible. Laboratory models of such systems offer a promising approach to test hypothetical scenarios for the origin of cellular life.

Introduction

Nucleic acid replication, transcription, and protein synthesis are characteristic of all contemporary forms of life, but such highly evolved processes could not have played a role in the steps leading to the origin of molecular systems having the properties of the living state. Instead, we must consider simpler physical processes that are collectively referred to as self-assembly. Certain organic molecules have properties that allow them to spontaneously organize into larger structures, a common example being the self-assembly of amphiphilic soap molecules into soap bubbles. All living cells are defined by membranes, and the same forces that act between soap molecules also stabilize membrane boundaries between the cytoplasm and the external environment.

Two other self-assembly processes play central roles in all life today. The first is the folding of amino acid polymers into highly ordered structures of functional proteins. This folding process occurs when amino acids are linked into proteins on ribosomes, and the folded state is stabilized by physical forces acting between the amino acids that compose the polymer. If protein-like molecules were somehow produced on the early Earth, they would also have the capacity to fold into a variety of structures, some of which could perform catalytic functions in primitive forms of life.

The second basic self-assembly process involves base pairing in nucleic acids, which is stabilized by hydrogen bonding between complementary bases. The resulting intra- and intermolecular forces produce structures such as hairpins and helices in DNA and RNA. Base pairing also plays a role in catalyzed DNA replication when nucleotides in solution bind specifically to complementary bases in templates. All life today depends on such self-assembly processes, and the earliest forms of life must have had primitive versions incorporated in their molecular systems.

Our current understanding of self-assembly processes in contemporary cellular life leads to a variety of hypothetical scenarios about how life can begin on a planetary surface.19 Given the presence of liquid water, there is little doubt that mixtures of organic compounds present on prebiotic Earth would become organized into more complex systems by self-assembly. Such microscopic molecular systems can be thought of as countless natural experiments that would occur globally for tens of millions of years prior to the origin of life. The next step toward life would take place when a few such systems happened to contain the particular set of molecules that allowed capture of energy and nutrients from the environment to be used for polymer synthesis. As noted earlier, polymer synthesis defines growth in all living systems today, and a molecular system capable of such reactions is well on its way toward the living state. Significantly, if one of the growing systems contained molecules that could be used as templates to direct further growth, a second polymeric molecule could be synthesized that was a replica of the



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