The origin and early evolution of life in chemical composition space.

Highlights • Chemical composition space helpfully summarizes chemical disequilibria • Life states are metastable attractors that convert food and energy into their key components • New life likely originates at interfaces between low and high diffusion phases (e.g., submerged mineral surfaces) • Chance changes in composition can move a life state to a new, potentially fitter, state • Adaptive evolution in surface-associated life predicts and the origin of cells Abstract Life can be viewed as a localized chemical system that sits in the basin of attraction of a metastable dynamical attractor state that remains out of equilibrium with the environment. To explore the implications of this conception, I introduce an abstract coordinate system, chemical composition (CC Space), which summarizes the degree to which chemical systems are out of equilibrium with the bulk environment. A system's chemical disequilibrium (CD) is defined to be proportional to the Euclidean distance between the composition of a small region of physical space, a pixel, and the origin of CC space. Such a model implies that new living states arise through chance changes in local chemical concentration (“mutations”) that cause chemical systems to move in CC space and enter the basin of attraction of a life state. The attractor of a life state comprises an autocatalytic set of chemicals whose essential (“keystone”) species are produced at a higher rate than they are lost to the environment by diffusion, such that spatial growth of the life state is expected. This framework suggests that new life states are most likely to form at the interface between different physical phases, where the rate of diffusion of keystone species is tied to the low-diffusion regime, whereas food and waste products are subject to the more diffusive regime. Once life nucleates, for example on a mineral surface, it will tend to grow and generate variants as a result of additional mutations that find alternative life states. By jumping from life state to life state, systems can eventually occupy areas of CC space that are too far out of equilibrium with the environment to ever arise in a single mutational step. Furthermore, I propose that variation in the capacity of different surface associated life states to persist and compete may systematically favor states that have higher chemical disequilibrium. The model also suggests a simple and predictable path from surface-associated life to cell-like individuation. This dynamical systems theoretical framework provides an integrated view of the origin and early evolution of life and supports novel empirical approaches. Graphical abstract Image, graphical abstract [ABSTRACT FROM AUTHOR]