Life's Order, Complexity, Organization, and Its Thermodynamic-Holistic Imperatives

Life (Basel). 2012 Nov 13;2(4):323-63. doi: 10.3390/life2040323.

Abstract

In memoriam Jeffrey S. Wicken (1942-2002)-the evolutionarily minded biochemist, who in the 1970/80s strived for a synthesis of biological and physical theories to fathom the tentative origins of life. Several integrative concepts are worth remembering from Wicken's legacy. (i) Connecting life's origins and complex organization to a preexisting physical world demands a thermodynamically sound transition. (ii) Energetic 'charging' of the prebiosphere must precede the emergence of biological organization. (iii) Environmental energy gradients are exploited progressively, approaching maximum interactive structure and minimum dissipation. (iv) Dynamic self-assembly of prebiotic organic matter is driven by hydrophobic tension between water and amphiphilic building blocks, such as aggregating peptides from non-polar amino acids and base stacking in nucleic acids. (v) The dynamics of autocatalytic self-organization are facilitated by a multiplicity of weak interactions, such as hydrogen bonding, within and between macromolecular assemblies. (vi) The coevolution of (initially uncoded) proteins and nucleic acids in energy-coupled and metabolically active so-called 'microspheres' is more realistic as a kinetic transition model of primal biogenesis than 'hypercycle replication' theories for nucleic acid replicators on their own. All these considerations blend well with the current understanding that sunlight UV-induced photo-electronic excitation of colloidal metal sulfide particles appears most suitable as a prebiotic driver of organic synthesis reactions, in tight cooperation with organic, phase-separated, catalytic 'microspheres'. On the 'continuist vs. miraculist' schism described by Iris Fry for origins-of-life considerations (Table 1), Wicken was a fervent early protagonist of holistic 'continuist' views and agenda.