The origin of cellular life

This essay presents a scenario of the origin of life that is based on analysis of biological architecture and mechanical design at the microstructural level. My thesis is that the same architectural and energetic constraints that shape cells today also guided the evolution of the first cells and that the molecular scaffolds that support solid-phase biochemistry in modern cells represent living microfossils of past life forms. This concept emerged from the discovery that cells mechanically stabilize themselves using tensegrity architecture and that these same building rules guide hierarchical self-assembly at all size scales (Sci. Amer 278:48-57;1998). When combined with other fundamental design principles (e.g., energy minimization, topological constraints, structural hierarchies, autocatalytic sets, solid-state biochemistry), tensegrity provides a physical basis to explain how atomic and molecular elements progressively self-assembled to create hierarchical structures with increasingly complex functions, including living cells that can self-reproduce.     

The early evolution of cellular life

Recent progress in data collection and analysis has changed the study of origin of life from an area dominated by speculation into a field abundant with testable hypotheses. This review discusses advances in the following areas: the fossil recordsd; the 'retrodiction' of biochemical pathways; and contradictions between different molecular phylogenies. The latter indicates a limited number of horizontal gene transfers during the early evolution. However, these cases of horizontal gene transfer are so infrequent that they can be detected as exceptions in an otherwise coherent picture. Cases of horizontal gene transfer can be recognized within the background of the majority consensus of molecular markers. The fusion of separate lineages to form new species is revealed by the simultaneous horizontal transfer of several independent genes.     

Driving forces in the origins of life

What were the physico-chemical forces that drove the origins of life? We discuss four major prebiotic ‘discoveries’: persistent sampling of chemical reaction space; sequence-encodable foldable catalysts; assembly of functional pathways; and encapsulation and heritability. We describe how a ‘proteins-first’ world gives plausible mechanisms. We note the importance of hydrophobic and polar compositions of matter in these advances.     

The chemical origins of life and its early evolution: an introduction

Can we look at contemporary biology and couple this with chemical insight to propose some plausible mechanisms for the origin of life on the planet? In what follows, we examine some promising chemical reactions by which the building blocks for nucleic acids might have been created about a billion years after the Earth formed. This could have led to self-assembling systems that were based on an all-RNA metabolism, where RNA is both catalytic and informational. We consider the breadth of RNA enzymes presently existing in biology, and to what extent these might have covered a wider range of chemistry in the RNA world. Ultimately, the RNA world would probably have given way to protein-based life quite quickly, and the origins of peptidyl transferase activity are discussed below.     

DNA and the origins of life in micaceous clay

Reproducible imaging of DNA by atomic force microscopy was a useful predecessor to Ned Seeman’s DNA nanotechnology. Many of the products of DNA nanotechnology were imaged in the atomic force microscope. The mica substrate used in this atomic force microscopy research formed the inspiration for the hypothesis that micaceous clay was a likely habitat for the origins of life. Montmorillonite clay has been a successful substrate for the polymerization of amino acids and nucleotides into peptides and DNA oligomers in research on life’s origins. Mica and montmorillonite have the same anionic lattice, with a hexagonal spacing of 0.5 nm. Micas are nonswelling clays, with potassium ions (K⁺) holding the crystal sheets together, providing a stable environment for the processes and molecular complexes needed for the emergence of living cells. Montmorillonite crystal sheets are held together by smaller sodium ions (Na⁺), which results in swelling and shrinking during wet-dry cycles, providing a less stable environment. Also, the cells in all types of living systems have high intracellular K⁺ concentrations, which makes mica a more likely habitat for the origins of life than montmorillonite. Finally, moving mica sheets provides mechanical energy at the split edges of the sheets in mica “books.” This mechanical energy of mica sheets, moving open and shut, in response to fluid flow, may have preceded chemical energy at life’s origins, powering early prebiotic processes, such as the formation of covalent bonds, the interactions of molecular complexes, and the budding off of protocells before the molecular mechanism of cell division had developed.     

The photochemical origins of life and photoreaction of ferrous ion in the archaean oceans

A general argument is made for the photochemical origins of life. A constant flux of free energy is required to maintain the organized state of matter called life. Solar photons are the unique source of the large amounts of energy probably require to initiate this organization and certainly required for the evolution of life to occur. The completion of this argument will require the experimental determination of suitable photochemical reactions. Our work shows that biogenetic porphyrins readily photooxidize substrates and emit hydrogen in the presence of a catalyst. These results are consistent with the Granick hypothesis, which relates a biosynthetic pathway to its evolutionary origin. We have shown that photoexcitation of ferrous ion at neutral pH with near ultraviolet light produces hydrogen with high quantum yield. This same simple system may reduce carbon dioxide to formaldehyde and further products. These reactions offer a solution to the dilemma confronting the Oparin-Urey-Miller model of the chemical origin of life. If carbon dioxide is the main form of carbon on the primitive earth, the ferrous photoreaction may provide the reduced carbon necessary for the formation of amino acids and other biogenic molecules. These results suggest that this progenitor of modern photosynthesis may have contributed to the chemical origins of life.