Emergence of life: Physical chemistry changes the paradigm

Origin of life research has been slow to advance not only because of its complex evolutionary nature (Franklin Harold: In Search of Cell History, 2014) but also because of the lack of agreement on fundamental concepts, including the question of ‘what is life?’. To re-energize the research and define a new experimental paradigm, we advance four premises to better understand the physicochemical complexities of life’s emergence: 1. Chemical and Darwinian (biological) evolutions are distinct, but become continuous with the appearance of heredity. 2. Earth’s chemical evolution is driven by energies of cycling (diurnal) disequilibria and by energies of hydrothermal vents. 3. Earth’s overall chemical complexity must be high at the origin of life for a subset of (complex) chemicals to phase separate and evolve into living states. 4. Macromolecular crowding in aqueous electrolytes under confined conditions enables evolution of molecular recognition and cellular self-organization. We discuss these premises in relation to current ‘constructive’ (non-evolutionary) paradigm of origins research – the process of complexification of chemical matter ‘from the simple to the complex’. This paradigm artificially avoids planetary chemical complexity and the natural tendency of molecular compositions toward maximum disorder embodied in the second law of thermodynamics. Our four premises suggest an empirical program of experiments involving complex chemical compositions under cycling gradients of temperature, water activity and electromagnetic radiation.