Energetic Constraints on H₂-Dependent Terminal Electron Accepting Processes in Anoxic Environments: A Review of Observations and Model Approaches

Abstract

Microbially mediated terminal electron accepting processes (TEAPs) to a large extent control the fate of redox reactive elements and associated reactions in anoxic soils, sediments, and aquifers. This review focuses on thermodynamic controls and regulation of H2-dependent TEAPs, case studies illustrating this concept, and the quantitative description of thermodynamic controls in modeling. Other electron transfer processes are considered where appropriate. The work reviewed shows that thermodynamics and microbial kinetics are connected near thermodynamic equilibrium. Free energy thresholds for terminal respiration are physiologically based and often near -20 kJ mol(-1), depending on the mechanism of ATP generation; more positive free energy values have been reported under "starvation conditions" for methanogenesis and lower values for TEAPs that provide more energy. H2-dependent methanogenesis and sulfate reduction are under direct thermodynamic control in soils and sediments and generally approach theoretical minimum energy thresholds. If H2 concentrations are lowered by thermodynamically more potent TEAPs, these processes are inhibited. This principle is also valid for TEAPS providing more free energy, such as denitrification and arsenate reduction, but electron donor concentration cannot be lowered so that the processes reach theoretical energy thresholds. Thermodynamics and kinetics have been integrated by combining traditional descriptions of microbial kinetics with the equilibrium constant K and reaction quotient Q of a process, taking into account process-specific threshold energies. This approach is dynamically evolving toward a general concept of microbially driven electron transfer in anoxic environments and has been used successfully in applications ranging from bioreactor regulation to groundwater and sediment biogeochemistry.

Drainage-induced forest growth alters belowground carbon biogeochemistry in the Mer Bleue bog, Canada

“…On the contrary, in the upper 100 cm of peat hydrogen concentrations were strongly elevated compared to concentrations at the 200 m reference site. Levels of H 2 concentration were also much higher than the 7-13 nmol L -1 H 2 that have typically been reported during ongoing steady state hydrogenotrophic methanogenesis in anaerobic environments (Heimann et al 2010;Lovley and Goodwin 1988).…”

“…It is important to distinguish between Gibbs free energies that (a) are typically attained during ongoing methanogenesis and (b) minimum energy requirements, or thermodynamic thresholds, at which the free energy provided by the process is insufficient for the generation of ATP (Heimann et al 2010). Gibbs free energies of -30 to -40 kJ mol -1 (CH 4 ) have been reported under ongoing hydrogenotrophic and acetoclastic methanogenesis in short-term anaerobic incubation experiments with sediments and rice paddy soils and temperatures of 15°C to room temperature (Chin and Conrad 1995;Rothfuss and Conrad 1993).…”

“…These substrates are provided by syntrophic interaction with fermenting bacteria (Conrad 1999). Rates of methanogenesis are diminished by microbial utilization of electron acceptors, other than CO 2 , because substrate concentrations are then lowered to levels that are thermodynamically inaccessible to methanogens (Heimann et al 2010;Hoehler 2004). According to Schink (1997), a critical energy of around -20 to -25 kJ mol -1 substrate is needed for hydrogenotrophic methanogenesis, representing the energy required for the generation of 1/3 ATP.…”

Reductive Dechlorination of Trichloroethylene (TCE) in Competition with Fe and Mn Oxides—Observed Dynamics in H2-dependent Terminal Electron Accepting Processes

“…Hydrogen threshold concentrations for different metabolic processes reported in previous experimental studies under a range of conditions are <0.1 nM for nitrate reduction; < 0.5 nM for Mn(IV) reduction; 0.1-0.8 nM during iron(III) reduction; 0.6-0.9 nM for TCE reduction, 0.1-2.5 nM for cis-DCE reduction and 2-24 nM for VC reduction; 1-15 nM H 2 for sulfate reduction, 5-100 nM and > 354 nM during methanogenesis and acetogenesis, respectively (Heimann et al, 2009;Löffler et al, 1999;Lovley and Goodwin, 1988;Lu et al, 2001;Luijten et al, 2004;Mazur et al, 2003;Yang and McCarty, 1998). These H 2 ranges suggest that TCE reduction may take place along with Fe(III) reduction followed by sulfate reduction.…”

Microbial services and their management: Recent progresses in soil bioremediation technology

“…In order for a reaction to take place the change of Gibbs free energy must be adequate. A bacterium needs a minimum of about -20 kJ per mol of substrate in order to exploit the free energy change in a reaction (Heimann et al, 2010;Schink, 1997). Estimates of the Gibbs free energy for several PAH (polycyclic aromatic hydrocarbons) indicate energetic yields between -209 and -331 kJ/mol for their methanogenic degradation under standard conditions, however this process has long been considered impossible (Dolfing et al, 2009).…”