Quantifying the energetics of metabolic reactions in diverse biogeochemical systems: electron flow and ATP synthesis


Corresponding author: D. E. LaRowe. Tel.: +31 30 253 3990; fax: +31 30 253 5302; e-mail: larowe@geo.uu.nl.


Classical solution chemistry and thermodynamics have been used to quantify the energetics of two fundamental bioenergetic processes over a range of environmental conditions in which life is known to thrive: (1) the flow of electrons originating from an electron donor through the nicotinamide adenine dinucleotide (NAD) redox couple to an electron acceptor, and (2) the synthesis of ATP from ADP and aqueous phosphate. The approach taken explicitly accounts for the chemical formulas, charge states, complexation of ADP and ATP with magnesium, and the thermodynamic properties of individual biochemical species in stoichiometric and charge-balanced reactions among biomolecules and other compounds. Because these species are represented in the reactions by explicit formula units, the chemical and thermodynamic consequences of the reactions can be evaluated as a function of temperature, pH, and bulk composition. To illustrate the utility of this approach, the energetics of the oxidation of glucose and hydrogen and the reduction of oxygen and sulfate coupled to NAD were characterized as functions of pH and temperature. The thermodynamic drive (chemical affinity, A) for glucose to reduce NAD increases as the temperature increases, whereas the opposite is true for hydrogen. Also, at lower pHs, the chemical affinity is lower for these two electron donors to reduce NAD than at higher pHs. Similarly, the chemical affinity for oxidation of NAD by oxygen decreases by more than 2 kcal mol−1 as temperature increases from 0 to 125 °C but the chemical affinity for oxidation of NAD by sulfate decreases by less than 1 kcal mol−1. Calculations were also carried out to quantify the energetics of the synthesis of ATP for different bulk compositions, pHs, and temperatures. The chemical affinity for the synthesis of MgATP from MgADP and aqueous monophosphate at pH 5 minimizes with increasing temperature from 0 to 125 °C, which is not the case at pH 7 or 9. The procedures employed in these various calculations can be used to better understand how different environmental variables influence biogeochemical interactions. In addition, they help constrain the minimum energy required to sustain a particular microbial population and provide the means to determine why certain types of metabolism occur in the environments in which they do.