Bioenergetic Conditions of Butyrate Metabolism by a Syntrophic, Anaerobic Bacterium in Coculture with Hydrogen-Oxidizing Methanogenic and Sulfidogenic Bacteria

Abstract

The butyrate-oxidizing, proton-reducing, obligately anaerobic bacterium NSF-2 was grown in batch cocultures with either the hydrogen-oxidizing bacterium Methanospirillum hungatei PM-1 or Desulfovibrio sp. strain PS-1. Metabolism of butyrate occurred in two phases. The first phase exhibited exponential growth kinetics (phase a) and had a doubling time of 10 h. This value was independent of whether NSF-2 was cultured with a methanogen or a sulfate reducer and likely represents the maximum specific growth rate of NSF-2. This exponential growth phase was followed by a second phase with a nearly constant rate of degradation (phase b) which dominated the time course of butyrate degradation. The specific activity of H 2 uptake by the hydrogen-oxidizing bacterium controlled the bioenergetic conditions of metabolism in phase b. During this phase both the Gibbs free energy (Δ G ′) and the butyrate degradation rate ( v ) were greater for NSF-2- Desulfovibrio sp. strain PS-1 (Δ G ′ = −17.0 kJ/mol; v = 0.20 mM/h) than for NSF-2- M. hungatei PM-1 (Δ G ′ = −3.8 kJ/mol, v = 0.12 mM/h). The Δ G ′ value remained stable and characteristic of the two hydrogen oxidizers during phase b. The stable Δ G ′ resulted from the close coupling of the rates of butyrate and H 2 oxidation. The addition of 2-bromoethanesulfonate to a NSF-2-methanogen coculture resulted in the total inhibition of butyrate degradation; the inhibition was relieved when Desulfovibrio sp. strain PS-1 was added as a new H 2 sink. When the specific activity of H 2 consumption was increased by adding higher densities of the Desulfovibrio sp. to 2-bromoethanesulfonate-inhibited NSF-2-methanogen cocultures, lower H 2 pool sizes and higher rates of butyrate degradation resulted. Thus, it is the kinetic parameters of H 2 consumption, not the type of H 2 consumer per se, that establishes the thermodynamic conditions which in turn control the rate of fatty acid degradation. The bioenergetic homeostasis we observed in phase b was a result of the kinetics of the coculture members and the feedback inhibition by hydrogen which prevents butyrate degradation rates from reaching their theoretical V max .

Physiology, Ecology, Phylogeny, and Genomics of Microorganisms Capable of Syntrophic Metabolism

“…of these compounds is exergonic. Consistent with the thermodynamic predictions, small increases in H 2 partial pressure inhibit the degradation of butyrate and benzoate by syntrophic cocultures 4,[16][17][18][19][20] and propionate degradation in methanogenic mixed cultures. 21 Since this first description of syntrophic metabolism, numerous studies have led to the isolation of many novel genera and species that are capable of syntrophic metabolism.…”

Thermodynamics of methanogenic intermediary metabolism in littoral sediment of Lake Constance

“…In other words, the degradation of valerate and caproate halted as soon as the AG of the reaction was higher than a critical amount of energy required for the degradation process. In the littoral sediment of Lake Constance these critical energies seemed to be smaller than -10 to -7 kJ mol-1 H2" Similar critical energies were observed for the H2-producing reactions in defined syntrophic cocultures [30,31] and in sewage sluge digestors [32]. Interestingly, the energy available for H2-dependent methanogenesis was in a similar range (about -9 kJ mo1-1 H2).…”

Kinetics of syntrophic cultures: A theoretical treatise on butyrate fermentation

“…From the measured threshold hydrogen concentration (63 Pa), they calculated an acetate concentration of 120 M and a corresponding free energy change of −26 kJ · mol −1 . Dwyer et al (1988) and Hickey and Switzenbaum (1991) measured butyrate conversion at free energy changes significantly closer to 0 kJ · mol −1 , but in their experiments the acetate concentration was much higher (>5 mM), and consequently the hydrogen concentration was lower. On the basis of our calculations we suggest that the low critical free energy change for butyrate fermentation observed by Wallrabenstein and Schink may be the result of kinetic limitations through hydrogen inhibition, and therefore their value may not represent a "true" critical free energy change.…”