The energetics of organic synthesis inside and outside the cell

Abstract

Thermodynamic modelling of organic synthesis has largely been focused on deep-sea hydrothermal systems. When seawater mixes with hydrothermal fluids, redox gradients are established that serve as potential energy sources for the formation of organic compounds and biomolecules from inorganic starting materials. This energetic drive, which varies substantially depending on the type of host rock, is present and available both for abiotic (outside the cell) and biotic (inside the cell) processes. Here, we review and interpret a library of theoretical studies that target organic synthesis energetics. The biogeochemical scenarios evaluated include those in present-day hydrothermal systems and in putative early Earth environments. It is consistently and repeatedly shown in these studies that the formation of relatively simple organic compounds and biomolecules can be energy-yielding (exergonic) at conditions that occur in hydrothermal systems. Expanding on our ability to calculate biomass synthesis energetics, we also present here a new approach for estimating the energetics of polymerization reactions, specifically those associated with polypeptide formation from the requisite amino acids.

Keywords: bioenergetics; biomolecule synthesis; hydrothermal systems; organic synthesis; polypeptide formation.

Figure 1.

Illustration of the range of oxidation states of carbon in common biomolecules and other organic compounds.

Figure 2.

Calculated consequences for carbon speciation of attaining metastable equilibrium states at 100°C in mixtures of seawater with submarine hydrothermal vent fluids of variable initial redox state on the early Earth (derived from results presented in Shock & Schulte [46]). In (a), the upward pointing arrow indicates conditions in a 100°C mixture of seawater and 350°C vent fluid initially at PPM, and the downward pointing arrow locates conditions prevailing in a 100°C mixture of seawater and 350°C vent fluid initially at FMQ. ‘Inorganic’ refers to the sum of dissolved CO₂, carbonate, bicarbonate and their complexes. In (b), numbers indicate carbon-chain length of n-carboxylic acids (2 = acetic acid, etc.).

Figure 3.

Gibbs energies (in joule per gram dry cell mass) of anabolic reactions that represent the sum total for cell biomass as a function of temperature in 12 deep-sea hydrothermal systems.

Figure 4.

Standard state Gibbs energy of polymerizing a mole of amino acids at saturation pressure, P_SAT, and at 500 bar from 0°C to 150°C.

Figure 5.

Gibbs energy required to polymerize a mole of protein consisting of the median number of amino acid residues in E. coli protein (278 AA residues) using the average concentration of protein in E. coli cytosol (8.7 µM) and various amino acid concentrations at saturation pressure from 0°C to 150°C.

Figure 6.

Gibbs energy of polymerizing a mole of protein of median amino acid residue length in the indicated organisms for concentrations of amino acids and protein equal to 6.5 mM and 8.7 µM, respectively, at saturation pressure from 0°C to 150°C.