Jan Spitzer | bioRxiv Science

bioRxiv2016

Complex molecular mixtures under cycling gradients as basis for lifes origins

We consider life as a cyclic physicochemical process that makes heredity and Darwinian evolution observable through living cells. We elaborate four principles that constrain current speculations about lifes emergence to natural processes driven by diurnal physicochemical gradients, primarily of temperature, water activity and electromagnetic radiation. First, Earths prebiotic chemical evolution is historically continuous with Darwinian evolution; second, cycling energies of solar radiation are primary drivers of chemical evolution; third, environmental molecular complexity must be high at the origin of life; and fourth, non-covalent molecular forces determine molecular recognition and cellular organization. Under normal physiological conditions of high ionic strength and high macromolecular crowding, hydration interactions (hydrogen bonding), screened electrostatic forces and excluded volume repulsions act over a commensurate distance of about one nanometer. This intermolecular distance governs chemical coevolution of proto-biomacromolecular surfaces (nucleic acids, proteins and membranes) toward Darwinian thresholds and living states. The above physicochemical principles of lifes emergence are consistent with the second law of thermodynamics, and with the current facts of molecular microbiology and planetary sciences. New kinds of experimentation with crowded molecular mixtures under oscillating temperature gradients - a PCR-like mechanism of lifes origins - can further illuminate how living states come about.\n\nGraphical abstractLifes emergence follows from chemical and Darwinian evolution, a high degree of molecular complexity and a high crowdedness, and non-covalent molecular forces that determine molecular recognition and cellular organization. The macromolecules divide the cytoplasm 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 (semi-conducting) electrolyte pathways of the crowded macromolecular regions.\n\n\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=103 SRC=\"FIGDIR/small/050740_fig1.gif\" ALT=\"Figure 1\">\nView larger version (36K):\norg.highwire.dtl.DTLVardef@1963682org.highwire.dtl.DTLVardef@d49be0org.highwire.dtl.DTLVardef@45ac46org.highwire.dtl.DTLVardef@312efc_HPS_FORMAT_FIGEXP M_FIG C_FIG

Microbiology↗

bioRxiv2013

Cycling Physicochemical Gradients as ‘Evolutionary Drivers’: From Complex Matter to Complex Living States

HighlightsO_LIBiological complexity cannot be reduced to chemistry and physics\nC_LIO_LIComplex living states are: multicomponent, multiphase, crowded, and re-emergent\nC_LIO_LILiving states arise naturally only by the action of cycling physicochemical gradients\nC_LIO_LIBacterial cells can be modeled as viscoelastic capacitors with sol-gel transitions\nC_LIO_LIEvolving living states can be investigated via biotic soup experimentation\nC_LIO_LIDarwinian evolution arises from the process errors of the cell cycle\nC_LIO_LISynthetic biology heralds the transition from unintentional Darwinian evolution to intentional anthropic evolution\nC_LI\n\nAbstractWithin the overlap of physics, chemistry and biology, complex matter becomes more deeply understood when high level mathematics converts regularities of experimental data into scientific laws, theories, and models (Krakauer et al., 2011. The challenges and scope of theoretical biology. J. Theoret. Biol. 276: 269-276). The simplest kinds of complex biological matter are bacterial cells; they appear complex-from a physicochemical standpoint-because they are multicomponent, multiphase, biomacromolecularly crowded, and re-emergent; the property of re-emergence differentiates biological matter from complex chemical and physical matter.\n\nBacterial cells cannot self-reassemble spontaneously from their biomolecules and biomacromolecules (via non-covalent molecular forces) without the action of external drivers; on Earth, such drivers have been diurnal (cycling) physicochemical gradients, i.e. temperature, water activity, etc. brought about by solar radiation striking the Earths rotating surface. About 3.5 billion years ago, these cycling gradients drove complex chemical prebiotic soups toward progenotic living states from which extant bacteria evolved (Spitzer and Poolman, 2009; The role of biomacromolecular crowding, ionic strength and physicochemical gradients in the complexities of lifes emergence. Microbiol. Mol. Biol. Revs. 73:371-388). Thus there is historical non-equilibrium continuity between complex dead chemical matter and complex living states of bacterial cells. This historical continuity becomes accessible to present-day experimentation, when cycling physicochemical gradients act on dead biomacromolecules obtained from (suitably) killed bacterial populations - on a biotic soup of chemicals (Harold, 2005, Molecules into cells: specifying spatial architecture. Microbiol. Mol. Biol. Rev. 69:544-564). The making of biotic soups and recovering living states from them is briefly discussed in terms of novel concepts and experimental possibilities.\n\nIn principle, emergent living states contingently arise and evolve when cycling physicochemical gradients continuously act on complex chemical mass; once living states become dynamically stabilized, the inevitable process errors of primitive cell cycles become the roots of Darwinian evolution.

Biophysics↗