The Role of Biomacromolecular Crowding, Ionic Strength, and Physicochemical Gradients in the Complexities of Life's Emergence

Abstract

SUMMARY We have developed a general scenario of prebiotic physicochemical evolution during the Earth's Hadean eon and reviewed the relevant literature. We suggest that prebiotic chemical evolution started in microspaces with membranous walls, where external temperature and osmotic gradients were coupled to free-energy gradients of potential chemical reactions. The key feature of this scenario is the onset of an emergent evolutionary transition within the microspaces that is described by the model of complex vectorial chemistry. This transition occurs at average macromolecular crowding of 20 to 30% of the cell volume, when the ranges of action of stabilizing colloidal forces (screened electrostatic forces, hydration, and excluded volume forces) become commensurate. Under these conditions, the macromolecules divide the interior of microspaces into dynamically crowded macromolecular regions and topologically complementary electrolyte pools. Small ions and ionic metabolites are transported vectorially between the electrolyte pools and through the (semiconducting) electrolyte pathways of the crowded macromolecular regions from their high electrochemical potential (where they are biochemically produced) to their lower electrochemical potential (where they are consumed). We suggest a sequence of tentative transitions between major evolutionary periods during the Hadean eon as follows: (i) the early water world, (ii) the appearance of land masses, (iii) the pre-RNA world, (iv) the onset of complex vectorial chemistry, and (v) the RNA world and evolution toward Darwinian thresholds. We stress the importance of high ionic strength of the Hadean ocean (short Debye's lengths) and screened electrostatic interactions that enabled the onset of the vectorial structure of the cytoplasm and the possibility of life's emergence.

Soft interactions and crowding

“…Charge-charge interactions also play a role. The environment inside E. coli is anionic (Spitzer and Poolman 2009). GB1 has a negative charge at physiological pH whereas NmerA and ubiquitin have insignificant net charge, making the latter two more 'sticky'.…”

The integration of activity in saline environments: problems and perspectives

“…However, based on studies primarily of bacteria, it is first and foremost, neither a dilute aqueous solution nor a sack of enzymes and metabolites interacting by random diffusion. It is, instead, highly crowded (Verkman 2002;Spitzer and Poolman 2005;van den Bogaart et al 2007;Spitzer and Poolman 2009). When biomacromolecules occupy 20-30% of the cytoplasmic volume (the normal situation) it becomes highly structured with spatially and temporally self-constructing molecular devices.…”

“…Both screened and unscreened electrostatic forces play important roles in the regulation of metabolism and transport. This crowding was probably essential to the evolution of life and is essential for its continuation (Spitzer and Poolman 2009).…”

“…For example, cyclic metabolic and replicative reactions can only occur in the cytosol within certain ranges of stabilising non-covalent forces as determined by ionic strengths (Spitzer and Poolman 2009); interestingly, when these are studied in vitro, ionic strength is typically adjusted using NaCl. The stabilising forces are determined in part by the distance from a particle or surface over which mobile charge carriers can screen out the external electric field, i.e.…”

Mineralization and non-ideality: on nature’s foundry

“…In view of the physicochemistry of cellular life, 'microspaces' with multicomponent, multiphase and crowded conditions in aqueous electrolytes are presumed crucial for enabling sustained biochemical processes (Spitzer et al 2015;Spitzer and Poolman 2009). Such crowded and confined environments render macromolecular reaction rates and equilibria complex, especially in view of the heterogeneous composition of biological spaces (Zhou et al 2008).…”